GENETICS

INTELLECTUAL BACKGROUND TO DARWIN'S DISCOVERY

Like any good intellectual pursuit , the problem of Origins can be traced back to Greek
philosophers. World view of the time was one of an eternal world, or at least one where time
was cyclical; a steady state world; concepts of time were very different from ours today: issue
was on origins; evolution (change) was less of a concern (according to E. Mayr, The Growth of
Biological Thought, Harvard University Press).
Plato's ideas dominated this line of thinking for next approx. 2000 years; his dogmas had the
effect of being antievolutionary (but not by intention): Essentialism, belief in a constant eidos, a
form or fixed idea. This idea was distinct from the phenomenon of appearance: there is an ideal
professor and I am but an imperfect personification of that ideal; there is an ideal Brown
undergraduate and, alas, you are all imperfect examples varying around that Platonic ideal.
Animate cosmos, the universe is a living harmonious whole. A creative power, a demiurge (not a
god-like creator). "Soul". All of these ways of thinking probably stifled evolutionary thought; the
emphasis was on origins. That an evolutionary thinking did not emerge probably stemmed from
the fact that evolution would disturb the harmonious whole.
Aristotle, a great naturalist and the founder of Natural History. Nature passes from inanimate
objects through plants to animals on to man in a "great chain of beings"; perpetuated the
Platonic view of the fixity of species and held that the natural order was eternal and unchanging
These views, held in a world where time was cyclical, all stifled (or at least diverted attention
away from) mechanistic/evolutionary thinking.
Jump through the fall of Rome to Christianity: the Word was that of God written in the Bible;
again focus was on origins (Creation in Genesis), but now time was unidirectional: the earth
and organisms were created once, Christ died once and the Judgment day will come but once!
Despite linearity of time, the fixity of species was still held in the context of Creation. Platonic
essentialism was still influential: God created the heavens, the earth and the organisms and since
God was a perfect god, the natural world thus must fit a pattern: the Scala Naturae (a legacy of
the Aristotelian great chain of beings). All things that God conceived of , did exist and held their
fixed place in nature. God would not have conceived of a species and then not created it. This is
the essence of the concept of plenitude: as many organisms that could exist, did exist; this was
all for the good. Extinction was not possible because a perfect God would not have permitted it.
As we'll see, fossils might present a problem for plenitude.
Natural Theology (Natural Philosophy) developed as one path to god; Nature was studied for
the greater glory of God since one path to that God was through the contemplation of his works
(e. g. nature). Ironic that natural theology set the stage for evolutionary thinking rather than other
philosophers.
The scientific reawakening that took place in the 16th and 17th centuries further set the stage for
evolutionary thinking (Descartes, Newton). Cosmology discovered the infinity of space and
lead to the development of theinfinity of time. They still held onto creationism and Christianity,
but the advances in the physical sciences came to challenge the all-powerful God as having a
hand in everything. God created the world, but physical lawskept it running. Still a major
barrier to evolutionary thought was the inability to observe evolution. One could watch a rock
drop and explain the process; evolution had to be inferred and hence a mechanism for evolution
did not yet develop.
Advances in Natural Theology and Geology began to challenge the fixity of
species. Linnaeus was a voracious cataloguer "for the greater glory of God" (Systema Naturae,
1735). Collected widely throughout Europe and had huge shipments of material from all over the
world sent to him by students and colleagues. Became clear that some of his own varieties and
those sent to him from other areas were not the same. Variation was being forced upon the
Naturalists
The age of discovery throughout the 15, 16, 17th centuries also began to notice different
faunas in different parts of the world. Buffon wrote Histoire Naturelle: 35 volumes! (1749-1788)
notes on many of the species that Linneaus had catalogued. Developed the discipline
of Biogeography. If the Fauna from Noah's ark is what populated the earth after the flood,
different faunas were hard to reconcile: "what the heck are these things?" Fossils were also found
that were not now alive (not represented in Noah's ark): big trouble for the principle of plenitude.
Georges Cuvier (1796-1832), founder of paleontology and comparative anatomy, worked in the
strata of the Paris basin. Discovered many fossils and described the exact stratigraphy. Found
that the lower the strata,the more different the fossils were from the organisms today. Maybe
there were a few floods?? and man was involved in the last one??. This rationalization fit into
then widely held view of Catastrophism, periodic catastrophes that shaped the earth. His data
ultimately provided the best evidence for evolution, but he remained opposed to the concept to
his death.
Uniformitarionism, proposed by James Hutton (1785), was contrary to Catastrophism in that it
proposed that the forces that formed and shaped the earth were the forces that are acting today.
Erosion and sedimentary deposition have been going on for millennia: earth had "no vestige of a
beginning, no prospect of an end"
Uniformitarionism was made conceivable by William Smith, a British canal surveyor and
engineer, walked the English countryside following geological strata. Found that one could
follow strata for miles, and more importantly, each stratified bed had a different flora and fauna.
Claimed that stratigraphic record was a record of sequence of deposition and hence time (1815).
Put a temporal scale on the fossil discoveries.
Sir Charles Lyell, in Principles of Geology (1830), formalized Hutton's and Smith's work in
strong support of Uniformitarionism. Darwin read it on the Beagle. Had a major influence on
Darwin in thinking about gradual biological change.
Many of these ideas and new bits of data were converging at the end of the 18th and beginning
of the 19th centuries. The accumulating evidence initiated belief that organisms could change
over time. Now we need a MECHANISM. Lamarck set the Scala Naturae in motion. Extinction
was a problem, but "solved" by arguing that lower forms changed in to higher forms (thus up the
great chain of being) Philosophie Zoologique (1809).
As to mechanism, acknowledged that the environment was ever changing and created new
"needs" ("besoin") in the organism. The changing environment stimulated "activities" in the
organism to meet these needs. Important(1): the environment did not directly induce the new
characters, it stimulated the organism to enhance these characters. Important (2): no volition
invoked; stimulus was a "need" not a "desire". Came to be called the Inheritance of Acquired
Characteristics. Nevertheless, initiated thinking about the Descent from a common ancestor.
Darwin claims he got nothing useful from Lamarck's work. The milieu in which Darwin began
his scientific career, extinction was accepted, fossils were viewed as real evidence of previous
life. Evolution of species (in the sense of serious questions about the fixity of species) was being
considered. The patterns were in place; Darwin came up with the process.
Some Darwiniana: A devoted naturalist from an early age. Loved to ride and hunt and walk
outdoors. Heavily influenced by his grandfather (Erasmus Darwin) a successful doctor and
author of Zoonomia in which notions of evolution were described (heretical for that time). As a
teenager, Darwin was active in the Plinian Society, a discussion group seeking physical, rather
than supernatural, explanations for scientific phenomena. Manyfreethinking
democrats involved. Darwin presented his first scientific paper to this group and was intoxicated
by the notion of discovering previously unknown facts of nature. Probably fostered a critical
view of the world, rather than accepting the religious dogma of the day.
Darwin was part of a very comfortable family. His father, too, was a successful doctor and his
mother was a Wedgwood (the wealthy family of potters). Darwin was a brilliant naturalist, but a
poor student. He hated medical school and withdrew (couldn't stand the sight of blood). Went on
to Cambridge with intention of ultimately becoming a clergyman (a common profession for
respectable, affluent men). Squeaked through Cambridge overspending his allowance, but
developed important relationships with his botany professor, Henslow, with whom he frequently
"botanized"
Henslow recommended to the powers that be, that Darwin should be selected as the unpaid
naturalist aboard the Beagle, a navy ship involved in a variety of missions (e.g., charting the
South American coast). Darwin's father, Robert, felt that going on such a mission was a further
postponement of 'getting on with his life' and said "if you can find any man of common sense
who advises you to go I will give my consent"
Darwin found this consent in his uncle Josiah Wedgwood (mom's brother) and a meeting with
Josiah, Robert Darwin and son Charles settled the matter. Charles had previously declined the
offer to be the Beagle's naturalist, so he quickly dashed off to Cambridge and then London to
meet with the ships captain, Robert FitzRoy. The interview with FitzRoy went extremely well
and FitzRoy had insisted that he would not take as a naturalist anyone with whom he could not
get along well personally (good idea for a 2-4? year trip on a small ship). Voyage of the Beagle
1831-1836.
Darwin's road to discovery is a model for many (most) organismal biologists: sail around the
world for five years, read books, collect specimens, observed different lands and people, come
home and digest it all and write up a theory that is a cornerstone of human intellectual history.
All this occurred with some important help. John Gould, the ornithologist who was analyzing
the mocking birds Darwin had brought back from the Galapagos, pointed out (March, 1837) that
the birds were distinct between three different islands. Darwin later wrote in the Origin how
arbitrary the distinction was between different varieties and species. The fixity of species held by
the creationists and the essentialists, and along with it Darwin's concept of what a species is, was
forever changed. Reading (September, 1838) Malthus's Essay on the Principle of
Population (1798) which argued that unlimited growth in human populations would lead to
famine. This led him to realize that the favorable variations would tend to be preserved, i.e., a
"struggle for existence" would lead, over time, to the origin of species by Natural Selection.
Simultaneous discovery of the essential concepts of natural selection by Alfred Russel
Wallace (letter to Darwin in June 1858; see figure 1.3, pg. 9). Darwin had been amassing a huge
body of information to support his theory. He knew that his ideas were going to cause a stink, so
he had to overwhelm the opposition with his "big book". Wallace's letter initiated the publication
of an "abstract" (about 500 pages): 1859
Variation among individuals
Brought inter-species variability down to the intra-species level
The variation is heritable
Had no clear understanding of genetics, but pigeon breeding convinced him of all that he
needed to know: variation could be enhanced by selecting out of a variable population
More individuals are produced than can survive each generation
the more favored forms in this variation will be preserved
The fact of evolution was probably accepted reluctantly, but Darwin's theory of evolution by
natural selection was challenged continuously. Genetics was the
problem. Blending inheritance (like mixing paints) would homogenize all individuals and there
would be no variation on which to select. Even with the rediscovery of Mendel's laws, the
differences between species were seen as Mendelian mutants, so species arose by discrete
mutations and the gradual change inherent in natural selection was inconsistent with the view of
mendelism at the time (figure 1.7, pg. 14)
In the 1920's and following, R. A. Fisher, J. B. S. Haldane and Sewall Wright (figure 1.8, pg.
15) showed that the mechanism of natural selection could operate on mendelian factors, and
more importantly that manycontinuously varying traits had genetic bases that could be
"mendelized' (shown to be the combined effects of several loci). Thus a rigorous mathematical
and genetical body of theory was developed that provided overwhelming support for Darwin's
mechanism. This came to be known as the Modern Synthesis. The first half of this course will
deal with this Neo-Darwinian approach to Evolution.
2. THE EVIDENCE FOR EVOLUTION: AN OVERVIEW
Diversity and Adaptation
Not (by themselves) good evidence: genetic basis; creationism; Intellegent design theory
Change over Time
Fossil horses: Gradual changes in toe number, body size, skull morphology. Clear linear
(actually sequential hierarchical) sequence. Correspondence of Jaw/tooth morphology to habitat
changes.
Extinct/Extant mammals: the extinct forms on any continent are closely related to the extant
forms on that continent. Australia: extinct Tertiary mammals are mostly marsupials, as are the
extant ones. South America: extinct Quaternary mammals are prominently armadillos and sloths,
as in the extant fauna
Industrial melanism The peppered moth Biston betularia: Preindustrial times the melanic forms
were about 1% in museum collection; post industrial times the melanics had reached 90% in
some areas. Dramaticfrequency change of an allele at a single Mendelian locus in 100 years.
Kettlewell placed the different colored moths on tree trunks of different background color and
showed that bird predation was higher on the more visible form. Recent evidence indicates that
the moths don't always sit on the tree trunks and there are viability differences between the two
genotypes, but the dramatic frequency change is documented nonetheless: selection occurred.
Resistance to pesticides and antibiotics: resistant strains of insects and bacteria have emerged
in short periods of time after the application of the insecticide/antibiotic. Either the variant was
there and it was swept to high frequency or recurrent mutations arose that happened to be
resistant.
Microevolution and macroevolution. The fact of evolution can be documented at either of
these two dramatically different time scales. Both are change over time, both are evolution
Descent with Modification
Homology: Attributes of two organisms are homologous when they are derived from an
equivalent characteristic of the common ancestor: vertebrate forelimbs, DNA
sequences (figure 3.6, pg. 54).
Embryos look alike while adults look different. This was viewed by Darwin as "by far the
strongest single class of facts in favor" of evolution
Vestigial organs: pelvic girdle, leg bones in snakes; non-functional toes in horses (figure 3.9,
pg. 58).

Artificial selection Dogs all descended from Wolf-like ancestor, selectively bred to have
different traits. Pigeons (Darwin's example), also selectively bred; clear evidence for heritable
variation
Natural selection: Differential survivorship and/or reproductive success.
Convergence Australian marsupials; Succulent plants; Alpine plants

MOLECULAR GENETICS

The transmission rules of genetic material are of fundamental importance to the theory of natural
selection and to all components of population genetics. It is essential that you have a solid
background in the basics of molecular and mendelian genetics.
DNA is the genetic material. A phosphate sugar backbone with purine or pyrimidine bases
bound to the sugar moiety. In the double helix structure of DNA, Adenine pairs with Thymine
and Cytosine pairs with Guanine. A:T or C:G pairs are held together with hydrogen bonds, the
C:G pairing being stronger than the A:T pairing.
The eukaryotic Chromosomes are made up of chromatin which is about half protein (histones)
and half DNA. The DNA is coiled around the histones in a nucleosome structure, and these
strings of nucleosomes are then coiled upon themselves making the hierarchical packaging of the
genetic material very space-efficient. The prokaryotic "chromosome" (usually one per cell) does
not have the tight packaging of eukaryotic chromosomes, but is associated with various proteins.
The Central Dogma describes the general view that information transfer in genetics is
unidirectional from DNA to RNA to protein, and has come to refer to the general mechanisms by
which this information is retrieved.Transcription is the polymerization of a strand of RNA from
DNA by the enzyme RNA polymerase. Translation is the various mechanisms by which the
sequence of nucleotides in the RNA is translated into a polypeptide and requires transfer RNAs,
the messenger RNA, ribosomes, amino acids (among other things; see Table 2.1, Figure 2.3 pg.
25-26).
The original view of the central dogma was One gene=>One protein (one gene codes for the
production, through transcription and translation, of one protein). This has been modified to the
view of one gene => one polypeptide since some genes code for parts of a protein; and further
defined as one gene => one function, since some genes code for RNA products (ribosomal
RNA, transfer RNA) which clearly are not polypeptides.Protein genes can be structural (e.g.,
collagen in your skin); catalytic (e.g., amylase enzyme in your saliva). How would you classify
hemoglobin?? RNA genes can also be structural (ribosomal RNA), catalytic (RNase P acts as a
cleavage enzyme).
Gene structure in prokaryotes often takes the form of an operon which is a set of adjacent
structural and regulatory genes. The coding regions (= genes) are uninterrupted open reading
frames of DNA that are transcribed as one RNA and translated into distinct polypeptides. The
adjacent regulatory regions can alter the expression of the genes in response to specific signals
from the cell.
Gene structure in eukaryotes is quite different , most notably in that the coding regions are often
broken up into exons (expressed) and introns (intervening sequences). Other specific sequences
in the DNA can serve as promoter elements to stimulate transcription. The intron/exon structure
of eukaryotic genes means that after transcription into RNA (called the pre-messenger RNA), the
intron sequences in the RNA must be removed and the exon sequence spliced back together.
After splicing, the RNA is called the messenger RNA (or "mature" messenger RNA) and is
transported out of the cell nucleus into the cytoplasm where it will be transcribed into protein.
The translation process goes on at the ribosomes and woks according to the rules of the genetic
code. With 20 amino acids found in proteins and only 4 nucleotides (A,C,T,G), the DNA must
be read in blocks of 3 nucleotides to provide enough information to translate DNA into
polypeptides (4
1
only = 4 ; 4
2
= 16 [still 4 amino acids short]; 4
3
= 64 [more than needed]). The
very important result of the fact the 43 = 64 means the genetic code is a redundant code, i.e.,
some three-nucleotide "words" will translate into the same amino acid (see table 2.1 page 26).
This means that some nucleotide positions in the coding region of a gene will be silentwith
respect to the amino acid sequence that gets translated from that DNA -> RNA. "Silent" means
that if a mutation occured at such a position and changed the nucleotide, the resulting amino acid
sequence would still be the same (e.g., see the third position for Leu in the table). Other
sites will affect the amino acid sequence if mutated (see second positions for all codons in the
code). We can thus refer to two general types of nucleotide positions in the DNA of coding
regions silent or synonymous sites (if mutated, no amino acid change) and replacement or
nonsynonymous sites (if mutated, a different amino acid sequence will result).
If we tabulate all possible changes in a theoretical "random" coding sequence, 61 codons could
code for amino acids (3 codons of the 64 total code for stop codons) with 3 nucleotides per
codon = 183 nucleotides. Each of these 183 different types of positions could change 3 ways (A
could mutate to C, G or T; C could mutate to A, G or T, etc.) for a total of 549 possible types of
changes in a random coding sequence. If we now look at the genetic code and ask whether each
of these possible changes is a silent or a replacement site, the following is obtained: 1st
position: 4% silent, 96% replacement; 2nd position: 0% silent, 100% replacement; 3rd
position:69% silent, 31% replacement. This means that mutation at 3rd positions in codons will
be much less likely to affect protein sequence and hence much less likely to be subject to natural
selection (more later on Molecular Evolution).
The genome is the total genetic complement of the cell. In humans this is about
3 billion nucleotides in a haploid genome (sperm or egg cell). Given a rough estimate of 100,000
genes per genome and 1000 base pairs (bp) per gene, this adds up to 10
5
x 10
3
= 10
8
, or
only 10% of our genome!! What the hell is all the rest of it for?? Good question (more late on
Molecular Evolution), but it appears to be spacer DNA and repetitive DNA.
MENDELIAN GENETICS
Adult human (mice, fruit flies, etc.) are diploid organisms having received one set
of chromosomes from the mother and one from the father. Humans have 46 chromosomes in 23
pairs; each pair is made up of one maternal and one paternal chromosome. The sex
chromosomes are a "pair" in females (two X chromosomes), but in males the X and Y sex
chromosomes are very different in size. The other 22 pairs of chromosomes areautosomes.
The chromosomes need not segregate as a
"top" and "bottom" set together because there is independent assortment of chromosomes
during meiosis making many different possible combinations. Note that in the lower gamete,
there is no F locus. This is the case in males when there is no section of the Y that is homologous
to the X.
Crosses between genotypes are best diagrammed in a Punnet square. These are made by putting
all possible types of gametes of one parent along one side of the square and all possible types of
gametes of the other parent along the other side. The boxes are filled in by pairing gametes
together to make genotypes. In a cross of two AA homozygotes, all offspring are identical. In a
cross between two heterozygous Aa x Aa, each parent can produce two possible gametes: A or a.
In the cross the genotypes come out as 1:2:1 of AA:Aa:aa. In a two locus situation where the loci
are on separate chromosomes (unlinked) and each locus is heterozygous, each adult can
produce 4 different gametes: AB, Ab, aB and ab. These four gametes go along each edge of a
4x4 Punnet square resulting in 16 possible 2-locus genotypes: AABB, AABb. AaBB, etc (figure
2.6, pg. 32). How would the Punnet square be different if the two parents had these genotypes:
AABb x AaBB? Work it out!
An important issue for Darwin was the mode of transmission of traits. The Lamarkian view of
the "inheritance of acquired characteristics" was workable under the Darwinian view, but was
wrong. Before the rediscovery of Mendel's work at the turn of the century, blending
inheritance was accepted mainly because offspring tended to look like a mixture of parents. But
note that if blending inheritance was the mechanism, then all individuals in the population would
eventually come to look alike and there would be no variation upon which to select! and Natural
Selection would not operate. This troubled Darwin to his death. Unfortunately Darwin never
found out about Mendel's experiments even though they were published long before Darwin's
death. Mendel's proposal of a "particulate" mechanism of inheritance solved the problem but the
history of Darwinism would have been interestingly different if Darwin had understood genetics
before he died. A simple example of a cross between a red (RR) and a white (rr) flower
illustrates the point: RRxrr gives all Rr (lets say they are pink). Now a cross of two pink flowers:
RrxRr gives back the parental types 1:2:1 RR:Rr:rr. The blending is a function of gene
expression, not gene inheritance (figures 2.8, 2.9, pg. 35, 37).

MUTATION AND VARIATION

Mutation is the ultimate source of variation. Without variation there could be no
evolution, so mutations are of great importance to evolution. Important to point out
that existing variation can be reshuffled by a variety of mechanisms that we don't
always consider as mutations leading to increases or decreases in variation and thus
altering the potential for evolution.
Mutation = a heritable change. This is often followed by the qualifier "in the DNA"
or "in the genetic material". This is redundant with the term "heritable" but points out
an important genetic issue: The mutations which are of primary concern are those in
the germ line as these are the one that will be passed on. August Weismann was the
first to point out the distinction between germ and soma. Mutations in your arm or
knee cap are not going to get passed on because the germline is sequestered relatively
early in development:
SOMA SOMA SOMA SOMA
GERM / -----> GERM / -----> GERM / -----> GERM / ----->
Weismann's doctrine was a serious blow to Lamarkian inheritance of acquired
characteristics. However, in plants and some animals (clonal ones in particular) the
germline is not sequestered into a single part of the part of the organism so somatic
mutations can be inherited (a mutation during the differentiation of a branch on
which a flower will develop: all pollen and ovules made by that flower will have a
genotype different from the rest of the plant. Think about corals, too).
Probably one of the most important things to understand about evolution is
that mutation is random, i.e., is not directed towards the problems presented by the
environment (although some recent evidence has been published on bacteria that
challenges this assumption: Lenski, R. E. Are some mutations directed? Trends in
Ecology and Evolution vol. 4, pp. 148-150.).
Mutation is an ongoing process. There are measurable mutation rates and that there
can be a genetic variation for mutation rates; "mutator strains" of bacteria exist.
Mutations in the replication or repair machinery of DNA can alter mutation rates.
Types of mutation: point mutation now generally refers to a change at a single
nucleotide site. These can be transitions (purine to purine [A to G or G to A], or
pyrimidine to pyrimidine [C to T or T to C]) ortransversions (from a purine to a
pyrimidine or vice versa). Synonymous and non-synonymous substitutions with
respect to the effect on the amino acid coded for by the
DNA. Deletions and insertion will causeframeshift mutations.
Transposable elements are mobile genetic elements that can move from one part of
the genome to another. Generally they have repeated sequences at their ends and code
for protein(s) in the middle. In moving from one location to another they can cause
mutations. If the element landed in the middle of the coding sequence of a gene, it
most likely would lead to a frameshift mutation or introduce a stop codon, and knock
out the function of that gene.
Gene duplications can occur by unequal crossing over where gene families exist on
the chromosome, homologous chromosomes may misalign and cross over
(recombine). The daughter chromosomes include one with an extra copy and one with
one fewer copies. Chromosome rearrangements can also be viewed as mutations.
Classic cases: inversions were a section of the chromosome is inverted with respect to
the "normal" chromosome. Drosophila polytene chromosomes show characteristic
banding patterns and allow for easy recognition of inversions. A paradigm of natural
selection (more later).
Several important consequences: Inversions can act as suppressors of crossing
over in the heterokaryotype (= heterozygote for two different chromosomal types).
An inversion does not prevent crossing over per sebut the recombination products that
result from a crossover within the inversion either have two centromeres and are
pulled apart in division, or lack a centromere and are not transmitted. Only the
unrecombined parentalchromosomes are transmitted.
How will the frequency of an inverted chromosome in a population affect it role as a
suppressor of recombination? The more frequent the inverted type gets, it will be
present in a "homokaryotypic" state and recombination will not be suppressed. If the
"inverted" chromosome were fixed in the population (=100%) then we would no
longer consider it "inverted".
Translocations are instances where part of a chromosome is "translocated" = moved
to another chromosome. When entire chromosome arms are translocated or fused this
can lead to changes in chromosome number. Can also lead to genetic incompatibilities
that may lead to reproductive isolation (more in lectures on speciation)
LINKAGE AND RECOMBINATION
Gene loci on the same chromosomes are generally considered to be in the
same linkage group because the alleles on each chromosome can be inherited as a
"linked set" (like beads on the same string). But a chromosome can be long enough
that the probability of a crossover (=recombination) event some where along the
chromosome is very high. Thus genes at different ends of same chromosomes can
be effectively unlinked. Conversely genes close to each other on the chromosome are
usually tightly linked because the probability of a recombination event between them
is very low.
Consider a pair of chromosomes, and think about the gene loci at each ends. Each
locus carries two alleles and we will consider the c

PHENOTYPE AND GENOTYPE

Definitions: phenotype is the constellation of observable traits; genotype is the genetic
endowment of the individual. Phenotype = genotype + development (in a given environment). To
consider these in the context of evolutionary biology, we want to know how these two are
related. In a narrow "genetic" sense, the genotype defines the phenotype. But how, in and
evolutionary sense, does the phenotype "determine" the genotype?Selection acts on
phenotypes because differential reproduction and survivorship depend on phenotype. If the
phenotype affecting reproduction or survivorship is genetically based, then selection can winnow
out genotypes indirectly by winnowing out phenotypes.
How do we get from genotype to phenotype? Central dogma: DNA via transcription
to RNA via translation to protein; proteins can act to alter the patterns and timing of gene
expression which can lead tocytodifferentiation where cells take on different states; cell
communication can lead to pattern formation and morphogenesis and eventually we have an
adult!
Genotype is also used to refer to the pair of alleles present at a single locus. With alleles 'A' and
'a' there are three possible genotypes AA, Aa and aa. With three alleles 1, 2, 3 there are six
possible genotypes: 11, 12, 13, 22, 23, 33. First we must appreciate that genes do not act in
isolation. The genome in which a genotype is found can affect the expression of that genotype,
and the environment can affect the phenotype.
Not all pairs of alleles will have the same phenotype: dominance when AA = Aa in phenotype,
A is dominant, a is recessive. An allele can be dominant over one allele but recessive to another
allele. Model of dominancefrom enzyme activity: no copies produce no phenotype, one copy
produces x amount of product and two copies produces 2x then the alleles are additive and there
is no dominance (intermediate inheritance). If one copy of the allele produces as much product
(or has as high a rate of flux) as a homozygote then there is dominance. There are cases where
the heterozygote is greater in phenotypic value than either homozygote: calledoverdominance
Single genes do not always work as simply as indicated by a dominance and recessive
relationship. Other genes can affect the phenotypic expression of a given gene. One example
is epistasis ("standing on") where one locus can mask the expression of another. Classic example
is a synthetic pathway of a pigment. Mutations at loci controlling the early steps in the pathway
(gene 1) can be epistatic on the expression of genes later in the pathway (gene 3) by failing to
produce pigment precursors (e.g. albinos) A-> gene 1 -> B -> gene 2 -> C gene 3 -> Pigment
Genes can also be pleitropic when they affect more than one trait. The single base pair mutation
that lead to sickle cell anemia is a classic example. The altered hemoglobin sequence is not the
only effect: lower oxygen affinity=anemia; clogged capillaries=circulatory problems; in
heterozygote state=malarial resistance. Mutations in cartilage are another example since
cartilage makes up many different structures the effects of the mutation are evident in many
different phenotypic characters.
Polygenic inheritance can be explained by additive effects of many loci: if each "capital" allele
contributes one increment to the phenotype. With one locus and additive effects we have three
phenotypic classes: AA, Aa and aa. With two loci and two alleles in a strictly additive model
(i.e., no epistasis or other modifying effects) we can have five phenotypic
classes aabb<Aabb=aaBb<AaBb=AAbb=aaBB<AABb=AaBB<AABB and the intermediate
phenotypic values can be produced in more ways, so should be more frequent. The more loci
affecting the trait, the greater number of phenotypic classes.
PATTERNS OF VARIATION
Evolution by Natural Selection rests on the following principles:
1. there is variation in natural populations
2. the variation is heritable; has a genetic basis
3. more offspring are produced than will survive each generation: struggle for existence
4. if heritable variation affects survival/reproduction, there will be differential
reproduction=selection
Without genetic variation there will be no evolution. Thus, characterizing the genetic variation in
natural populations is fundamental to the study of evolution. (see The Genetic Basis of
Evolutionary Change by Lewontin , 1974)
What kinds of variation are there? Discrete polymorphisms (e.g., Biston betularia) easily
noticed, but not frequent or representative of the variation in natural populations (eye color in
humans also quasi discrete).Continuously varying traits can be described by the mean x = (
X
i
)/n and variance V = 1/n S(X
i
-x)
2
. Examples: the carrots in the Burpee Catologue; human
height. Continuously varying traits will have both a genetic and environmental components.
How much genetic variation is there? Historical debate: Classical school held that there was
very little genetic variation, most individuals were homozygous for a "wild-type" allele. Rare
heterozygous loci due to recurrent mutation; natural selection purges populations of their "load"
of mutations. Balance school held that many loci will be heterozygous in natural populations
and heterozygotes maintained by "balancing selection" (heterozygote advantage). Selection thus
plays a role in maintaining variation.
How do we measure variation? To show that there is a genetic basis to a continuously varying
character one can study 1) resemblance among relatives: look at the offspring of individuals
from parents in different parts of the distribution; can estimate heritability (more later).
2) artificial selection: pigeons and dogs show that there is variation present; does not tell how
much variation
Protein electrophoresis: phenotype = gene product of specific locus (loci). Took off in mid 60's
(Lewontin and Hubby, 1966; Harris, 1966); still used. Grind up organism in buffer, apply
homogenate to gel (starch, acrylamide), apply electric field, proteins migrate in gel according to
charge, stain gel with histochemical stain for enzyme activity, bands reveal variation. Do this for
many loci and can estimate: proportion of loci polymorphic per population (10-60%,
depending on organism); proportion of loci heterozygous per individual (3-20% depending on
organism). The technique provides a minimum estimate because different amino acid sequences
may migrate at the same rate in the gel.
DNA variation. Measure the genetic material directly; sequencing is the most precise but the
most laborious; restriction enzyme analysis faster but has less information. These techniques
have revealed that there is even more genetic variation that what was revealed by protein
electrophoresis. Hence the debate between the Classical and Balance schools of genetic variation
has evolved into a debate about the forces maintaining genetic variation: the Neutralist-
Selectionist controversy (or debate). Some loci are neutral; others under selection (more in
lecture on Molecular Evolution). The debate is not over.
How is variation apportioned within and among populations? Hierarchy in patterns of variation:
are populations either melanistic or normal; or do populations contain some of both; if so what
are the frequencies in different populations? Is the variation within or among populations?
Spatial Patterns of Variation
Geographical isolates: discontinuous or disjunct distribution. Is there differentiation?Are there
continuous distributions, clinal variation, abrupt discontinuities ("step" cline).

INTRODUCTION TO POPULATION GENETICS
In this and the next few lectures we will be dealing with population genetics which generally
views evolution as changes in the genetic makeup of populations. This is a somewhat
reductionist approach: if we could understand the combined action of the forces that change gene
frequencies in populations, and then let this run over many generations we might understand
long term trends in evolution. Continuing debate: can the processes of microevolution account
for the patterns of macroevolution? Population genetics is an elegant set of mathematical
models developed by largely by R. A. Fisher and J. B. S. Haldane in England and Sewall Wright
in the US. Continues to be developed by many mathematical, theoretical and experimental
biologists today (see J. Crow and M. Kimura Introduction to Population Genetics Theory).
In very simple terms, population genetics involves analyses of the interactions between
predictable, "deterministic" evolutionary forces and unpredictable, random, "stochastic" forces.
The deterministic forces are often referred to as "linear pressures" because they tend to push
allele frequencies in one direction (up, down or towards the middle). Important forces of this
nature are selection, mutation, gene flow, meiotic drive (unequal transmission of certain alleles
[a form of selection]), nonrandom mating (also a form of selection). The primary stochastic
evolutionary force is genetic drift which is due to the random sampling of individuals (and
genes) in small populations. It is important to realize that the deterministic forces may act
together or against one another (e.g., selection may "try" to eliminate an allele that is pushed into
the population by recurrent mutation). Moreover, deterministic forces may act with or against
genetic drift, to determine the frequencies of alleles and genotypes in populations (e.g., gene
flow tends to homogenize different populations while drift tends to make them different). Hence,
the interaction of these forces is what we are really interested in (a later lecture), but since this
can get very complex mathematically, we will start by analyzing one force at a time.
To begin we need to understand some simple population genetic "bookkeeping." Consider
a locus with two alleles (alternative forms of the DNA sequence that "reside" at that locus, e.g.,
one from mother other from father). Now consider a population of N individuals (N=population
size); this means that there are 2N alleles in the population. We can thus talk about genotype
frequencies and allele frequencies. In a population of N = 100 individuals, if there are 25 AA,
50 Aa and 25 aa, then the genotype frequencies are f(AA) = 0.25, f(Aa) = 0.50 and f(aa) = 0.25.
If we count up the individual alleles there are 200 of them (because there are
100diploid individuals). Hence to determine the frequency of the "A" allele we have to count
each individual "A" allele that is specified in each diploid genotype. We get f(A) = (25+25+50) /
200 = 0.5. We generally refer to the frequency of the "A" allele as f(A) = p; the frequency of the
"a" allele is f(a) = q. Note that p = (1-q) because the sum of the allele frequencies must be 1.0.
Common "language errors" in learning population genetics are to refer to the "p" allele when you
really mean the "A" allele, or to say "the frequency of the p allele" when you really mean: "...p,
the frequency of the "A" allele..." Got it?? Good.
Since evolution is change in the genetic makeup of a population over time, a general approach to
modeling this is to determine the allele and genotype frequencies in the next generation (p
t+1
)
that result from the action of a force on those frequencies in the current generation (p
t
). Thus :
p
t
-> evolution happens -> p
t+1

Consider a simplistic life cycle where the genotypes (a single locus way of referring to adults)
produce gametes. These gametes mate to form new genotypes (=adults). See 5.1, pg. 93 and 5.3,
pg. 99. The relationship between allele frequencies (sometimes called "gene" frequencies) and
genotype frequencies is determined by the Hardy Weinberg Theorem which defines the
probabilities by which gametes will join to produce genotypes. Consider a coin toss: probability
of a head = 0.5; of a tail = 0.5; prob. of two heads = 0.5x0.5 = 0.25; prob. of one head and one
tail = 0.5x0.5 = 0.25, etc. Each coin is analogous to the type of allele you can get from one of
your diploid parents; the tossing of two coins is analogous to the mating of two individuals to
produce four possible genotypes (but heads,tails is the same as tails,heads). Now consider a roll
of the dice. The probability of each face is 1/6, and is actually analogous to cases where more
than two different alleles exist in the population at a given locus. The probability of any
combination is 1/6 x 1/6 = 1/36. But recall that there can be more than one way to get many of
the combinations (2,3 is the same as 3,2). The general expression for the number of genotypes
that can be assembled from n different alleles is: [n(n+1)/2].
Assumptions of Hardy Weinberg: 1) diploid sexual population 2) infinite size, 3) random
mating, 4) no selection, migration or mutation. This is a Null Model; obviously some of these
assumptions will not hold in real biological situations. The theorem is useful for comparison to
real-world situations where deviations from expectation may point to the action of certain
evolutionary forces (e.g., mutation selection, genetic drift, nonrandom mating, etc.). Use a
Punnet square to determine genotype frequencies: f(AA) = p
2
, f(Aa) = 2pq, f(aa) = q
2
and p
2
+
2pq + q
2
= 1 Learn this: One generation of random mating restores Hardy Weinberg
equilibrium. H-W equilibrium is when the genotype frequencies are in the proportions expected
based on the allele frequencies as determined by the relation p
2
+ 2pq + q
2
. This is derived more
thoroughly in table 5.1, and accompanying text, pg. 94.
Example: consider a sample of 100 individuals with the following genotype frequencies:

Observed Genotype
Frequencies
Allele count Allele frequency
Expected genotytpe frequencies
under H-W
BB 0.71 142 B p = 156/200 = 0.78 p
2
= (.78)
2
= 0.61
Bb 0.14 14 B, 14 b

2pq = 2(.78)(.22) = 0.34
bb 0.15 30 b q = 44/200 = 0.22 q
2
= (.22)
2
= 0.05
Observed are different from expected, thus some force must be at work to change frequencies.
NATURAL SELECTION
Selection occurs because different genotypes exhibit differential survivorship and/or
reproduction. If we consider a continuously distributed trait (e.g., wing length, weight) with a
strong genetic basis, the response to selection can be characterized by where in the distribution
the "most fit" (greatest survivorship&reproduction) individuals lie. If after selection one
extreme is most fit this is directional selection; if the intermediatephenotypes are the most fit
this is stabilizing selection; if both extremes are the most fit this is disruptive selection.
R. A. Fisher proposed a simple bookkeeping, or population genetics, approach for one locus with
two alleles: we have AA, Aa and aa in frequencies p
2
, 2pq, q
2
. Define l
ii
as the genotype-specific
probability of survivorship, mii as the genotype-specific fecundity. We build a model that will
predict the frequencies of alleles that will be put into the gamete pool given some starting
frequencies at the preceding zygote stage;
Genotypes Zygote -----> -----> Adult -----> -----> Gametes
AA p
2


l
AA
p
2


m
AA
l
AA
p
2

Aa 2pq

l
Aa
2pq

m
Aa
l
Aa
2pq
aa q
2


l
aa
q
2


m
aa
l
aa
q
2

The gamete column is what determines the frequencies of A and a that will be put into the
gamete pool for mating to build the next generation's genotypes. We can simplify by referring to
the fitness of a genotype as w
ii
= m
ii
l
ii
. These fitness values will determine the contribution of
that genotype to the next generation. Thus the frequency of A allele in the next generation
p
t+1
(sometimes referred to as p') would be the contributions from those genotypes carrying the A
allele divided by all alleles contributed by all genotypes:
p
t+1
= (w
AA
p
2
+ w
Aa
pq)/(w
AA
p
2
+ w
Aa
2pq + w
aa
q
2
). Or for the a allele,
q
t+1
= (w
aa
q
2
+ w
Aa
pq)/(w
AA
p
2
+ w
Aa
2pq + w
aa
q
2
). Note that the heterozygotes are not 2pq
but pq because in each case they are only being considered for the one allele in question. If we
scale all wii's such that the largest = 1.0 we refer to these as the relative fitnesses of the
genotypes. A worked example where p = .4, q = .6 and w
AA
= 1.0 w
Aa
= 0.8 w
aa
= 0.6:
Genotype frequencies are p
2
= 0.16, 2pq = 0.48, q
2
=0.36, thus:
p
t+1
= ((.16 x 1.0) + (.24 x .8))/((.16 x 1.0) + (.48 x .8) + (.36 x .6)) = .463; so q = .537 and thus
f(AA)
t+1
= .215, f(Aa)
t+1
= .497 and f(aa)
t+1
= .288. Note both allele frequencies and genotype
frequencies have changed (compare to what we saw with inbreeding). This can be continued
with the new allele frequencies and so on. When will the selection process stop? when Ap = 0,
i.e., when p
t+1
= p
t
. In some situations this will stop only when one allele is selected out of the
population (p = 1.0).
Now we can consider various regimes of selection (s = selection coefficient, (1-s) is fitness):

AA Aa aa

I 1 1 1 - s selection against recessive
II 1 - s 1 - s 1 selection against dominant
III 1 1 - hs 1 - s incomplete dominance (0<h<1)
IV 1 - s 1 1 - t selection for heterozygotes

Substitute the fitnesses (w
ii
) in condition I above into the expression Ap = p
t+1
- p
t
and prove for
yourself that the equations on page 101 (eqn. 5.5) is related to the expression for p
t+1
shown
above. First three are directional in that selection stops only when allele is eliminated. In I the
elimination process slows down because as q becomes small the a alleles are usually in
heterozygote state and there is no phenotypic variance. In II selection is slow at first because
with q small most genotypes are AA so there is low phenotypic variance; as selection eliminates
A alleles q increases and the frequency of the favored genotype (aa) increases so selection
accelerates. III is like the worked example run to fixation/loss. IV is known as balancing
selection due to overdominance (heterozygotes are "more" than either homozygote). Both
alleles maintained in population by selection. This is an example of a polymorphic
equilibrium (fixation/loss is also an equilibrium condition but it is not polymorphic). The
frequencies of the alleles at equilibrium will be:
p
equil
= t/(s + t); q
equil
= s/(s+t).
Classic example = sickle cell anemia. A=normal allele; S=sickle allele. S should be eliminated
because sickle cell anemia lowers fitness. S is maintained where malarial agent (Plasmodium
falciparum) exists because AS heterozygotes are resistant to malaria. Note that S allele is very
low frequency where there is no malaria (the selective coefficient of S is different because
the environment is different). See figure 5.8, pg. 120; table 5.9, pg. 119.
Another way that genetic variation can be maintained is through multiple niche
polymorphism (polymorphism maintained by environmental heterogeneity in selection
coefficients). If different genotypes are favored in different niches, patches or habitats, both
alleles can be maintained.

AA Aa aa
habitat 1 1.0 0.8 0.5
habitat 2 0.5 0.8 1.0
Heterozygotes will have the highest average fitness although they are not the most fit in either
habitat (see figure 5.12, pg. 124). The same dynamics would apply to temporal
heterogeneity (spring and fall; winter and summer) assuming that selection did not eliminate
one allele during the first period of selection. Classic example of temporal heterogeneity: third
chromosome inversions of Drosophila pseudoobscura studied by T. Dobzhansky. Different
chromosomal arrangements ("Standard" and "Chiricahua") show reciprocal frequency changes
during the year.
Yet another way to maintain variation by selection is through frequency dependent selection.
If an allele's fitness is not constant but increases as it gets rare this will drive the allele back to
higher frequency. See figure 5.9, pg. 121. Example: allele may give a new or distinct phenotype
that predators ignore because they search for food using a "search image" (e.g., I like the green
ones).
Most (by no means all) evolutionary biologists believe that selection plays a major role in
shaping organic diversity, but it is often difficult to "see" selection. One reason is that selection
coefficients can be quite small (1-s ~1) so the response to selection is small. When selection
coefficients are large Ap can be large, but the problem here is that with directional selection
fixation is reached in a few generations and we still can't "see" selection unless we are lucky
enough to catch a population in the middle of the period of rapid change.
What affects the rate of change under selection? Recall that Ap = p
t+1
- p
t

Ap = [(w
AA
p2 + w
Aa
pq)/(w
AA
p2 + w
Aa
2pq + w
aa
q2)] - p . With some simple algebra we can
rearrange this
equation to: Ap = (pq[p(w
AA
- w
Aa
) + q(w
Aa
- w
aa
)])/(w
AA
p2 + w
Aa
2pq + w
aa
q2)
Note that Ap will be proportional to the value of pq. This value (pq) will be largest when
p=q=0.5 or, in English, when the variance in allele frequency is greatest. This is a simplified
version of the main point of thefundamental theorem of natural selection modestly presented
by R. A. Fisher.

It states that the rate of evolution is proportional to the genetic variance of the population. In
the above example we have not explicitly defined the fitnesses wiis or the dominance
relationships and these can have a major effect on Ap as written above.
Another important observation for looking at this Ap equation and plugging in some values is
that selection always increases the mean fitness of the population. For example with p=0.4,
q=0.6 and w
AA
=1, w
Aa
=0.8 and w
aa
=0.6, the mean fitness (w'bar') = 0.76. After one generation of
selection p' = 0.463 and q' = 0.537. Recalculating w'bar' we get wbar
t+1
= 0.78, which is greater
than 0.76. When will this process stop? At fixation (or equilibrium with overdominance).
This treatment of the algebra of natural selection illustrates what selection alone can do to allele
and genotype frequencies. In the next lectures we will consider other evolutionary forces
(mutation gene flow, genetic drift), how they act alone, and eventually, how they interact with
each of the other evolutionary forces.
MUTATION AND MIGRATION
We have learned how selection can change the frequencies of alleles and genotypes in
populations. Selection typically eliminates variation from within populations. (The general
exception to this claim is with the class selection models we have called "balancing" selection
where alleles are maintained in the population by overdominance, habitat-specific selection, or
frequency dependent selection). If selection removes variation, soon there will be no more
variation for selection to act on, and evolution will grind to a halt, right? This would be true if it
were not for the reality of Mutation which will restore genetic variation eliminated by selection.
Thus, mutations are the fundamental raw material of evolution.
We will be gin by considering what mutation will do as an evolutionary force acting by itself.
Simply, mutation will change allele frequencies, and hence, genotype frequencies. Lets consider
a "fight" between forward and backward mutation. Forward mutation changes the A allele to the
a allele at a rate (u); backward mutation changes a to A at a rate (v). We can express the
frequency (p) of the A allele in the next generation (p
t+1
) in terms of these opposing forward and
reverse mutations, much like forward and reverse chemical equations: (p
t+1
) = p
t
(1-u) +
q
t
(v). The first part on the right is accounts for alleles not mutated (1-u), and the second part
accounts for the increase in p due to mutation from a to A (the frequency of a times the mutation
rate to A). We can also describe the change in allele frequency between generations (Ap) as: Ap
= (p
t+1
) - (p
t
). This is useful because it lets us calculate a theoretical equilibrium
frequency which is defined as the point at which there is no more change in allele frequencies,
i.e. when Ap = 0 which is when (p
t+1
) = (p
t
); from above: p
t
(1-u) + (1-p)
t
(v) = p
t
[remember,
q=(1-p)]. Now solve for p and convince yourself that the equilibrium frequency = p = v/(u+v).
Similarly the equilibrium frequency of q = u/(u+v).
MUTATION AND SELECTION BALANCE
In the real world we will generally not find specific evolutionary forces acting alone; there will
always be some other force that might counteract a specific force of interest. Our ability to detect
these opposing evolutionary forces depends, of course, on the relative strengths of the two (or
more) forces. However, it is instructive to examine the conditions where evolutionary forces
oppose one another to give us a feel for the complexity of evolutionary processes. Here we will
consider a simple case where mutation introduces a deleterious allele into the population and
selection tries to eliminate it.
As above we define the mutation rate (u) as the mutation rate to the "a" allele. This will tend to
increase the frequency of a (i.e., q will increase). In fact, q increases at a rate of u(1-q);
remember, (1-q) = p, or the frequency of the A allele. This mutation pressure will increase the
number of alleles which selection can act against.
To select against the a allele, we first will assume complete dominance, i.e., that the deleterious
effects of the a allele are only observed in the aa homozygote. Under these conditions, the
frequency of "a" (q) decreases by selection at a rate of -sq
2
(1-q), where s is the selection
coefficient. We won't derive this for you, but note that the amount of change generated by this
selection is a function of the frequency of the aa homozygote (q
2
) and the frequency of the A
allele (1-q). In other words, the amount of change is proportional to the amount of genetic
variation in the population, as we showed last lecture.
If we put these terms for mutation and selection together, the amount of change in the a allele is :
Aq = u(1-q) - sq
2
(1-q)
Now, if the "fight" between selection and mutation is a "draw", we have a condition where there
is no change in the frequency of the a allele since mutation is increasing q just as fast as selection
is reducing it. Under these conditions, Aq = 0, and we say that the equilibrium allele
frequency, q-hat, has been reached (in formal notation q-hat is q with a circumflex over it). We
simply rearrange the above formula so that is becomes : u(1-q) = sq
2
(1-q). We solve this for q to
give the equilibrium allele frequency , q-hat: q = sqrt(u/s) (sqrt stands for square root).
Most mutation rates are fairly small numbers (about 10
-6
), so this equation suggests that
deleterious alleles will be maintained in mutation selection balance at fairly low frequencies.
However, this statement is exactly what this mode is intended to illustrate: we cannot say what
that frequency is until we know BOTH mutation rate and selection coefficient. However, we will
refer back to mutation selection balance several times during the course, so it is essential that you
have a feel for dynamics of this evolutionary interaction.
MIGRATION
In population genetics, the term "migration" is really meant to describe Gene flow, defined as the
movement of alleles from one area (deme, population, region) to another. Gene flow assumes
some form of dispersal or migration (wind pollination, seed dispersal, birds flying, etc.)
but dispersal is not gene flow (genes must be transferred, not just their carriers)
We can describe gene flow (migration) in a manner similar to mutation. Consider two
populations, x and y with frequencies of the A allele of px and py . Now consider that some
individuals from population y migrate into population x. The proportion of these y individuals
that become parents in population x in the next generation = m. After the migration event,
population x can be considered to consist of migrant individuals (proportion m) and non-migrant
individuals (proportion [1-m]). Thus the frequency of the A allele in population x in the next
generation (px t+1) is just the frequency in the non-migrant portion (= px [1-m]) plus the
frequency in the migrant portion (py m). Thus: px t+1 = px t [1-m] + py m.
The change in allele frequency due to gene flow is Ap = (px t+1) - px t which is just;
[px t [1-m] + py m] - px t Multiplying through and canceling terms leaves us with:
Ap = -m(px t - py t). This makes intuitive sense: the change in p depends on the migration
rate and the difference in p between the two populations. If we considered a grid or array of
populations and focus on one of those populations as the recipient population with all other
populations contributing equally to it, then py would be replaced by the average p for all the
other populations. Many scenarios are possible.
GENE FLOW AND SELECTION
To address the combined effects of gene flow and selection, we will invoke a "fight" similar to
what we described for mutation selection balance above. Consider that some weak allele is
wafting over to the other side of the tracks, so to speak, where they do not survive (e.g., fish
swimming into New York harbor). There is an evolutionary pressure changing allele frequencies
in one direction ( into the harbor), and an opposing evolutionary force eliminating those alleles
(sewage killing off genetically intolerant fish). Depending on the relative strengths of these two
opposing forces, an equilibrium condition can arise.
Lets consider the movement of the "a" allele, and assume that it is completely recessive in its
phenotype of death-by-sewage. The change in allele frequency from the migration into the
harbor can be defined as above: Aq = -m(qx t - qy t). (Note that we have changed p to q since we
are considering the a allele; x and y refer to the two populations). The change in allele frequency
due to selection against this allele is -sq
2
(1-q) (note that this is the same expression we used in
the mutation selection balance above). Putting these two pieces together, we can write the
expression for the change in allele frequency that is due to BOTH gene flow and selection: Aq =
-m(qx t - qy t) - sq
x
2
(1-q
x
). When the "fight" between gene flow and selection is a "draw", the
system will be in equilibrium and there will be no change in q,
and -m(qx t - qy t) = sq
2
(1-q).
So, back to the fish. Lets say that aa homozygotes drop dead the minute they enter the East river
(but that AA and Aa fish are fine). Outside New York Harbor, the frequencies of the two alleles
are equal (p = q= 0.5). It is discovered that in the East river, q = 0.1 over many generations, and
the Mayor wants to know what proportion of the fish in the East river come from the outside
each generation. This information gives us all we need: it's in equilibrium, q
x
= 0.1 (East River),
q
y
= 0.5 (outside), and s = 1.0 since the aa's are dead. Plug in the values and you get m = 0.023.
This says that 2.3% of the fish in the East river must come from outside each generation to
maintain the allele frequency at q = 0.1
GENETIC DRIFT
Genetic drift refers to random fluctuations in allele frequencies due to chance events
(see figure 6.4, pg. 142). The previous lectures have all dealt with deterministic
(predictable) evolutionary forces often referred to as linear pressures. Genetic drift is a
stochastic (random) force that can scramble the predictable effects of selection,
mutation, and gene flow. While it might seem that a random force would be of little
significance to evolutionary "progress" (we'' confront this loaded term later), genetic
drift is an extremely important force in evolution. However, its strength depends on
the size of the population, as a simple exercise in coin tossing will illustrate. In ten
tosses you might easily get seven heads; in 1000 tosses, however, you would never get
700 heads with a "fair" coin. The same sort of random fluctuation in allele
frequencies can occur in small populations: consider a bag full of red and green
marbles each in equal frequency; pull out a small handful and the frequency in your
hand will probably not equal the frequency in the original bag. Let that handful
determine the frequency in a new population that grows back to the original
population size. A second small handful will randomly shift the frequency to yet
another frequency. If you pulled out all the marbles in the bag (= large population)
then the frequency would be maintained exactly in the next generation. Genetic drift is
not a potent evolutionary force in very large randomly mating populations.
To illustrate the consequences of genetic drift we will consider what happens when
drift alone is altering the frequencies of alleles among many small populations. To
illustrate this we need to understand Population structure, which describes how
individuals (or allele frequencies) in breeding populations vary in time and space.
This structure is determined by the combined effect of deterministic and stochastic
forces. We will introduce the idea of population structure by showing how genetic
drift and inbreeding can change the frequencies of genotypes in populations.
Consider a grid of small populations (e.g., ponds in Minnesota), all with the same
small population size and all starting at time t with p = q= 0.5. Through time each
population will experience genetic drift due to random sampling and the frequencies
in each population will diverge. The distribution of frequencies changes over time
from a tight distribution (all 0.5), to a flat distribution (some populations at p = 0.1,
some at 0.9 and all frequencies in between), to fixation (p =1.0) or loss (p = 0.0) of
the alleles in all populations (see figure below). Fixation is when all alleles in the
population are A; this necessarily implies loss of the a allele ("fixation" or "loss"
should only be used with reference to a specific allele). If each population starts at p =
0.5, then at the end, when all populations have lost their variation, 50% of the
populations will be fixed for the A allele and 50% will be fixed for the a allele (latter
= "loss" for the A allele, get it?). If the initial frequency was p = 0.7, then 70% of the
populations would be fixed for the A allele (again, assuming no selection, migration,
mutation).
Main Points: 1) total variation does not change; variation goes from within
populations (no variation between populations) to between populations (no
variation within populations). 2) genetic divergence of populations entirely
by chance! (no selection). This is why genetic drift can be an important force in
evolution.

At the start of this drift process in our array of populations, p = 0.5 and there are 2pq =
0.5 = 50% heterozygotes. When all populations in the array have fixed or lost the
allele, there can be no heterozygotes (i.e., 0%). This shows that the proportion of
heterozygotes decreases as drift proceeds (this also occurs when there is inbreeding
which can also be thought of as a sampling error phenomenon). We can quantify this
process as follows: the proportion of heterozygotes in the "next " generation is a
function of the proportion of heterozygotes in the present generation and the "rate" at
which drift proceeds: Ht+1 = Ht[1 - (1/2N)] where H = the proportion of heterozygotes
in the population (or in the array of populations) and N = population size. This can be
extended over many generations as follows: Ht = H0[1 - (1/2N)]t where t refers to the
number of generations in the future and 0 refers to the present (or starting) generation.
Looking at these equations it is clear that with small population sizes, heterozygosity
will be lost quickly (drift will proceed quickly), whereas in large populations there
will be little loss of heterozygosity.
If we consider our grid of populations again, we note that as drift proceeds and each
deme
becomes a bit different from every other deme, the variation among demes increases.
Like the loss of heterozygosity due to drift, the increase in the variation among demes
depends on the population size. This variation can be described as Vt = p(1-p)[1 - (1 -
1/2N)t]. Note at t=0, Vt = 0 because the term in brackets = 0. As the number of
generations proceeds, the variation among populations (Vt) increases rapidly if N is
small, but slowly if N is large.
A general result as drift proceeds in small populations is a deficiency of
heterozygotes, and reciprocally, an excess of homozygotes. This is also a common
result when there has been inbreeding (= mating between relatives). In fact genetic
drift and inbreeding are related phenomena. The relation between the frequencies
of expected versus observed heterozygotes allows us to determine the inbreeding
coefficient, F = (He - Ho)/He (subscripts e and o mean expected and observed,
respectively).
One effect of inbreeding is to increase the frequency of homozygotes (and thus,
necessarily, decrease the frequency of heterozygotes). Note: while the frequency
of genotypes change with inbreeding, the frequencies ofalleles remains the same
(assuming no selection, migration, mutation). Refer back to the data table presented
on page 2 of Lecture 6 to convince yourself that those data could be a result of
inbreeding: F=(0.343 - 0.14)/0.343 = 0.59. When the allele frequency is not zero, but
there is a complete absence of heterozygotes , F = 1. As an exercise, work through the
data in table 5.2, pg.98. Does this illustrate high or low inbreeding?
Genetic variation is generally "lost" by the action of genetic drift. This is true if we
follow the fate of one deme over time. Note, however, that in our array of populations,
variation is "lost" within demes, but the variation in the total system is preserved, i.e.,
the allele frequency in the entire metapopulation does not change, only the genotype
frequencies and allele frequencies within individual demes).
Inbreeding also has the effect of increasing the variance among the individual demes
of a larger population. As such, drift and inbreeding are closely related evolutionary
forces. Recall that the variance = 1/N_(X-xi)2. In a random mating population with p
= 0.4, f(AA) = 0.16, f(Aa) = 0.48, f(aa) = 0.36. If the alleles act in
an additive manner, the heterozygotes will be intermediate and close to the mean in
phenotype and will contribute little to the variance; with inbreeding most individuals
are homozygous, and thus would deviate from the mean and the variance would be
greater. In effect, inbreeding makes the distribution of phenotypes more "bimodal" by
essentially redistributing the alleles from all three genotypes into the two
homozygotes (see figure 6.5, pg. 143).
Population structure is usually quantified by a simple statistic known as Fst. This
stands for the "fixation" index resulting from comparing sub populations to the total
population, and is used to quantify the proportion of genetic variation that
lies between subpopulations within the total population. An important way of thinking
of this problem is to compare the mean heterozygosity averaged across all demes to
the heterozygosity that would result if all demes were pooled into one big population.
Heterozygosity is the proportion of heterozygotes in the population and is defined as
H = 2 p q. Note that heterozygosity is zero at "fixation", the case where only one
allele exists (p = 0 or 1), and that heterozygosity is at a maximum when alleles are
equally frequent (e.g., p = q = 0.5). [For completeness, H = 1- (p2 + q2) which follows
from Hardy-Weinberg above. In the case of more than two alleles, we can't just use p
and q, so the following expression for heterozygosity works more generally: H = 1 -
_xi2 where xi is the frequency of the "ith" allele, and summation is across all i alleles.
The expression 1 - (p2 + q2) is identical to 1 - _xi2 when there are only two alleles].
In our metapopulation example above, on the left all demes have p = 0.5 and the allele
frequency for the entire array is also p = 0.5. Right away you can se that there in no
differentiation among demes. To quantify this we use Fst which is calculated as Fst =
(Ht - meanHs) / Ht, where Ht = 2 (pooled p) (pooled q) [note that pooled q = (1-pooled
p)], and meanHs = the average of H values for each of the individual demes (i.e., 2 p q
for each deme, averaged across all demes). For the left-hand metapopulation Ht =
2(0.5)(0.5) = 0.5, and meanHs = 0.5 also. Thus , Fst = (0.5 - 0.5) / 0.5 = 0.0. What does
this mean? In English this says that none of the variation in this system of demes
lies between demes; the population structure is zero. Since there is variation (i.e., p _
0) all of the variation lies within demes.
Now consider the metapopulation system on the right above. The pooled allele
frequency is 0.5 because half of the demes are fixed for the A allele (p = 1.0) and half
are fixed for the a allele (p = 0.0). Hence the Ht value is 2 (pooled p) (pooled q) =
2(0.5)(0.5) = 0.5. The meanHs value is very different. Each deme has a heterozygosity
of zero (either p or q is zero in all demes), so the average Hs value is 0.0. Hence, for
the metapopulation on the right, Fst = (0.5 - 0.0) / 0.5 = 1.0. In English this means
that all (100%) of the variation in the system lies between the demes. By definition
then, none of the variation lies within demes, which we know because the little circles
are either filled or empty. By now it should be apparent that in Fst values can range
between the two extremes of zero and one that we have just illustrated. As genetic
drift proceeds, Fst values will increase, but the balance between drift and "linear
pressures" will determine what equilibrium Fst reaches (later lecture).
A further clarification: The "speed" or "intensity" of genetic drift is actually
determined by the effective population size (Ne). This may differ from the total
population size (N) if some individuals do not breed. Two examples where Ne differs
from N are cases of different mating system and temporal fluctuations in population
size. When the number of breeding males (Nm) _ number of breeding females (Nf),
the effective population size can be quite different from the actual population size.
The relation is: Ne = 4NmNf/(Nm + Nf). If Nm = Nf = N/2, then Ne = N. But if a
single male does all the mating (approximated in elephant seals) then Ne = 4 (because
Nf/(1+Nf) is approx. = 1). So the population genetics of elephant seals and sage
grouse will be very different from that of large populations of insects.
With population bottlenecks where the population size drops to a small number in
one generation, the effective population size is not just the average of N's for each
generation. To estimate the Ne, one calculates theharmonic mean population size as
follows:
1/Ne = 1/t_1/Nt where t = the number of generations and Nt = the population size at
each generation. Thus with population sizes of 100, 100, 20, 100 the arithmetic mean
= 80 but 1/Ne = 1/4(1/100 + 1/100 + 1/20 + 1/100) = 1/4(0.08) = 0.02, so Ne = 1/0.02
= 50. Thus the smaller population size has a disproportionate effect on the effective
population size. This is a very important issue in conservation efforts concerning
endangered species.
DRIFT AND MUTATION
Drift will tend to reduce heterozygosity (for our purposes this equals the proportion of
heterozygotes), mutation will introduce new alleles which will serve to increase
heterozygosity. This provides yet another example of a "fight" between opposing
evolutionary forces. When the mutation rate is close to the reciprocal of the
population size, heterozygostity will be high (i.e., a considerable amount of variation
will exist in the population). The "balance" of this equilibrium can be described by an
equation for the equilibrium frequency of heterozygotes:
H Plug in Ne's and u's to determine balance: when Ne = 1/u, H = 0.8; when
u>1/Ne then heterozygosity will be higher; when u<1/Ne heterozygosity will be
lower.
DRIFT AND GENE FLOW
Gene flow can counteract the loss of heterozygosity due to drift as well as counteract
the random divergence of allele frequencies among populations. The balance between
these two opposing forces can be described by an equation for the equilibrium
variance among populations
V(among pops.) . As m increases, the variance decreases (faster homogenization);
as Ne increases, the variance decreases (drift acts more slowly with larger Ne). Major
conclusion is that it takes very little gene flow to keep two "populations"
homogeneous, as little as one reproductive migrant between populations per
generation! See figure 5.13, pg. 128.
A number of different methods have been developed to estimate migration rates from
standing patterns of allele frequency variation. This rests on the fact that Fst values
are a result of a "balance" between gene flow and drift. One can calculate Fst from
molecular markers, and if an estimate of effective population size is available,
migration can be estimated from the following relation: Fst 1/(4Nem + 1). By
rearranging the formula and plugging in trial values you can see that low values for m
result in high values for Fst, and high values of m give low values of Fst. This follows
from the homogenizing effect of gene flow on allele frequency variation among
populations.
The nature of population differentiation can depend on population structure. Typical
scenarios include a Continent-Island model (gene flow from continent to island),
an Island model (equal probability of gene flow among several/many
populations), Stepping Stone model (gene flow is sequential among
populations), Continuous Model (e.g., carpet of individuals). In all cases (except
Island model) there can be Isolation by Distance simply reflecting incomplete
homogenization of populations due to incomplete flow of genes among all
populations.

INTEGRATION OF EVOLUTIONARY FORCES

Selection leads to an increase in the average fitness of the population. Illustrated by the
following example. Recall that the average fitness ("w bar") = w
AA
p
2
+ w
Aa
2pq + w
aa
q
2
. Now
consider the case where p=.2, q= .8 so f(AA)=0.04, f(Aa)=0.32 and f(aa)=0.64. If their respective
fitnesses are 1.0, 0.2 and 0.1, then w bar = .04(1)+.32(.2)+.64(.1) = .132. If selection were to
continue for a number of generations q would decrease and p would increase. Lets say that we
recalculated the average fitness when p=0.8 and q=0.2: thus f(AA)=.64, f(Aa)=.32 and f(aa)=.04
so w bar = .64(1)+.32(.2)+.04(.1)=.708. When will the average fitness reach a maximum? when
the deleterious allele (a) is selected out of the population so the only genotype is AA, the most fit
genotype. (How would this differ if there was dominance?)
The sickle cell story with a new twist. There are actually more than just two alleles relevant to
the sickle cell story. The normal allele (A) and the sickle allele (S) produce the genotypes
traditionally considered: AA is normal but susceptible to malaria, AS individuals are not severely
debilitated, but they are resistant to malaria, SS individuals are severely affected and rarely
survive to reproduce. A third allele (C) results in the following genotypes and phenotypes: AC is
normal but susceptible, SC has mild anemia and CC is normal and resistant to malaria. The
following approximate fitnesses have been assigned to these genotypes:
Genotype w phenotype
AA 0.9 malarial susceptibility
AS 1.0 malarial resistance
SS 0.2 anemia
AC 0.9 malarial susceptibility
SC 0.7 anemia
CC 1.3 malarial resistance
Bantu speaking people moved into central and western Africa. A slash and burn agriculture
opened up habitat for mosquitoes and along with them came Plasmodium the malarial agent.
Consider a large population with the above fitness exposed to malaria for the first time. f(A) ~
1.0 f(S) and f(C) very low, thus all S and C alleles will be in heterozygous states as AC or SC.
Virtually No SS or CC genotypes will be present (the product of two very small numbers).
Selection will lead to an increase of the S allele due to its higher fitness as a AS heterozygote.
Expect no change in the C allele because heterozygotes have equal or lower fitness than other
common genotypes. Can't "pass through" the heterozygote stage.

Selection is "short-sighted" cannot "see" the best solution, i.e., the highest fitness state where C
goes to fixation. How do we get to the "best" condition?
Consider the effects of population structure: Bantu people establish local breeding groups of
small effective population size. This necessarily will bring on some inbreeding which serves to
increase homozygotes and decrease heterozygotes. Some CC genotypes will be produced by the
chance effects of inbreeding and now the "best" genotype is present in the population and
selection can "see" it so the frequency of the C allele increases, and the population would go to
fixation for C.
The highest fitness state could not be reached by selection alone; Drift can affect the outcome
of selection. This has been conceptualized as an Adaptive landscape:

Pick two allele frequencies, one for the A locus and one for the B locus. This defines a
"population" (obviously this would be done in many dimensions for all loci in the genome; only
two here for illustration). The population will evolve by selection to the top of the nearest peak.
If a population starts with f(A) ~ f(B) ~ 0.2, this population would evolve to the top of the peak
at the lower right of the diagram. This is not the highest peak, but selection acts to increase
average fitness and can only "see" the nearest peak. If drift due to low effective population size
rapidly shifted both f(A) and f(B) to higher frequencies, then the population might be in
the "domain of attraction" of the highest peak in the upper right corner.
The population would stop evolving when it reached the top of the highest peak because there is
no higher peak to shift to unless the environment changes at which point we would have
to redraw the adaptive landscape.
Sewell Wright conceived of this view of evolution and believed that this was a more accurate
description of how "real" populations evolved sine most species do have some structure to their
populations and experience drift. So there will be a shifting balance between allele frequencies
and a shifting balance between drift and selection as the causative agents in evolution. This is the
so called shifting balance theory.
Wright envisioned different stages of evolution by shifting balance: 1) Drift in local
populations would shift allele frequencies to new values and the demes may evolve up a local
peak because the allele frequency in such a deme drifted near the 'domain of attraction' of a peak.
The assumption is that without drift, a population on a 'flat' section of the adaptive landscape
would not evolve by natural selection, because there would be no fitness variation in a flat region
of the landscape. 2) intrademic selection where selection within local populations (demes)
would drive the various demes to the top of their nearest peak. Even if several populations were
at different "locations" on the adaptive landscape, the highest peak may not be reached. One can
invoke stage 2.5 by saying that drift in local populations might move such a population's allele
frequency off one peak and into the 'domain of attraction' of an adjacent peak with a different
maximum fitness. This peak may be lower or higher than the old one, but after several rounds of
drift at least one population may evolve to the top of the highest peak. 3) This (these) high-
fitness populations will produce many emigrants and tend to change the other demes' allele
frequencies closer to their own as a result of gene flow; this third stage is called interdemic
selection(selection among demes); emigration rates are proportional to the extent that the fitness
of a given population is greater or less than the average fitness of all populations. When all
populations are homogenized to the allele frequencies of maximal fitness a new balance will be
achieved and the allele frequencies will be maintained by selection until the environment
changes the adaptive landscape. (For empirical support of this theory see Wade and Goodnight,
1991 Science vol. 253 pg. 1015-1018 and a commentary on page 973 by Crow).
Alternative way to view the shifting balance theory: consider a surface with troughs and pits in
it. Put several marbles on the surface. If marble is near pit it falls in selection ~ gravity. Shake
surface and balls will roll up out of pits against gravity and make their way to new
pit. Shaking ~ drift. See figures 8.8-8.11, pgs. 215-219.
Before discussing the shifting balance view of evolution we considered selection as if it were
acting on a single locus. This is a gross oversimplification because many loci are linked along
the chromosome. Who's to say that selection is acting the same way on both loci? Things get
much more interesting (but more complicated) when we face the reality of linked loci. Consider
the cross between the two two-locus genotypes:
The offspring can be AB/AB, AB/ab or ab/ab. Other two locus genotypes
are possible: or . But these can only be produced in the cross if there
is recombination between the two loci. We can thus refer to four two-locus gametes AB and ab
are the coupling gametes and aB and Ab are the repulsion gametes (another way to think about
gametes is to just refer to them as a "chromosome" since this will reflect the linear array of
whatever alleles are linked together). The frequency of these four gametes will be determined by
two things 1) the frequencies of the respective alleles (p and q for the A locus and a different p
and q for the B locus) and 2) the degree of linkage disequilibrium which describes whether
recombination has broken up any association between the two linked loci.
When allele frequencies all = 0.5 and all gametes are in equal frequency then f(AB) = f(ab) =
f(Ab) = f(aB). But if A alleles tend to be associated (linked) to B alleles then AB gametes will be
in higher frequency than expected at random. We can quantify the disequilibrium as follows:
D = [f(AB) f(ab)] - [f(Ab) f(aB)]. (Note frequencies are multiplied) When all gametes are in
equal frequency D = 0 i.e., linkage equilibrium. When only the coupling gametes are present D =
0.25; when only the repulsion gametes are present D = -0.25. If the frequencies of the alleles are
less than 0.5, then the maximum value for D will be less than 0.25.
Note that when allele frequencies are different from p = 0.5 = q, the maximum value of D
(absolute value)will be less than 0.25. For example if p=0.8, q=0.2 and if only the coupling
gametes were in the population then D = 0.16
A worked example: gamete frequencies in 1000 observations: 580 AB's, 140 Ab's, 60 aB's and
280 ab's. Thus f(A) allele = (520+140)/1000 = 0.66 so f(a) = .34. f(B) = (520+60)/1000 = 0.58 so
f(b) = 0.42. At random we expect the following gamete frequencies: f(AB) should be
.66(.58)1000 = 383. f(Ab) should be .66(.42)1000 = 277. f(aB) should be .34(.58)1000 = 197 and
f(ab) should be .34(.42)1000 = 143. These numbers of expected gametes are clearly different
from the observed gametes. We can thus calculate the linkage disequilibrium as d = [.52(.28)] -
[.14(.06)] = 0.1372. This tells us that the A and B alleles are in linkage disequilibrium.
This disequilibrium will be broken up by recombination and the rate of breakup will be
determined by the rate of recombination (see figure 8.2, pg. 202).
Now let's say that the A locus was under selection with A alleles favored. If the A and B loci
were in linkage disequilibrium in the coupling state what would happen to the B alleles? They
too would be selected for, but not because they were under selection. This is a very important
phenomenon in population and evolutionary genetics called hitchhiking. It demonstrates a very
important distinction we must make about selection and phenotype: we need to distinguish
between selection "of" and selection "for" If the A allele is favored, there is selection for the
A allele and selection of the B allele due to its linkage to the A allele (i.e., linkage between the A
and B loci).

Now consider the situation where the nose length is the result of interactions between the two
loci. In the first case the interaction is additive, in the second case there is epistasis

AA Aa aa

AA Aa aa
BB 1 2 3

BB 1 2 3
Bb 2 4 6

Bb 4 6 4
bb 3 6 9

bb 9 6 3
In the first case if we selected for long noses, we would tend to drive the a and b alleles to high
frequency. If we selected for long noses in the second case we would tend to drive the A and b
alleles to high frequency. The important distinction between these two tables is that in the
simple two-locus additive case on the left, heterozygotes at one locus are intermediate between
the two homozygotes regardless of the genotype at the other locus. In contrast, the table on the
right shows that the relationship between genotype and phenotype at one locus depends on the
genotype at the other, interacting locus. In a sense, one locus is modifying the expression of the
other locus. If selection were to act in favor of nose length in the right-hand epistatic system, the
way alleles "marched to fixation" would be very different.
Now consider how linkage and epistasis can affect the response to selection. In the second case
above if there was high linkage disequilibrium so that all we had we AB and ab chromosomes in
the population (= AB or ab gametes in the gamete pool), there would be less variation to select
on (sizes 1, 6 and 3). Now if there was recombination such that Ab and aB chromosomes were
produced, then the full range of phenotypic variation would be exposed (up to 9) and selection
would rapidly shift the mean phenotype to longer noses and to high frequency of A and b
alleles.
The general point is that loci do not act independently and their response to selection depends
critically on their linkage relationships and their interaction with other loci. For the
ecologically minded, there are some interesting parallels between community ecology and
population genetics: there are an uncountable number of ways that the interacting participants
can interact. In community ecology one considers species in a community; in population genetics
one considers genes in the genome. The fate of each player depends on the degree to which it is
"connected" to the other players in the system. Darwin referred to the complexity of nature as a
"tangled bank"; this is very true of the genes within genomes within populations.

QUANTITATIVE GENETICS

Quantitative genetics deals with the genetics of continuously varying characters. Rather than
considering changes in the frequencies of specific alleles of genotypes, quantitative genetics
seeks to "quantify" changes in the frequency distribution of traits that cannot easily be placed in
discrete phenotypic classes. The reason for the continuous variation is usually that the traits
are polygenic (controlled by many genes) and there areenvironmental effects that alter the
phenotypic state of each individual (see figures 9.3, 9.4, pgs. 226-227).
Consider two inbred strains that represent "extremes" of a phenotypic
distribution: high and low oil content in corn for example or long and short carrots. We will
assume that the plants of each type are homozygous at all loci. Under this assumption the
variation we see within each group is entirely environmental variation and the variation we
see between the two groups is mostly (but not entirely) genetic variation. If we then cross an
individual from the high group (ABCD) with an individual from the low group (abcd) we would
get F1 hybrids (ABCD/abcd) that are intermediate in phenotype. We would notice that each
individual is not identical in phenotype even though each is identical in genotype (all F1's). We
would then attribute all the variation in phenotype to an environmental component, VE. If we
than crossed all the F1's with each other, we would get an F2 distribution that would have
a wider distribution. Because of independent assortment of chromosomes and recombination in
the F1's each F2 is likely to have a unique multilocus genotype. Thus the total phenotypic
variance in the F2 distribution will have both a genetic component, VG and an environmental
component (VE). In simple terms, these are related by the expression VP = VG + VE.
If you were given a bunch of plants with a smooth continuous distribution of phenotypes, how
would you determine if there was a genetic basis to the variation? Simply select individuals from
the distribution with distinct phenotypes, breed them (=parents) and compare the phenotypes of
these parents to that of their offspring. If the mean phenotype of offspring was close to the mean
of the parents this would be evidence for a genetic basis for the phenotype and the trait would be
identified as heritable. If on the other hand, the offspring produced from two "high" parents
were extremely variable in phenotype and offspring produced from two "low" parents were
extremely variable there would be a weak genetic component to the trait. The heritability in a
"broad" sense can be expressed as the proportion of the total phenotypic variance that has a
genetic component: h
2
B = VG/VP. (see figures 9.5 pg. 231; 9.6 pg. 237).
This correlation between parent and offspring can serve as a simple means of quantifying the
heritability of the trait: if there is a 1:1 correlation of phenotype between parents and offspring
(e.g., a 45 degree slope of the regression of offspring phenotype vs. parent phenotype) then the
trait has the maximal heritability. With no relation between parents and offspring (a slope of
zero) the heritability would be zero (see box 9.1 pg. 233).
The genetic component of the variation can be broken up into different subcomponents. Consider
a simple additive model of beak size where the number of B alleles you have determines the size
of your beak: BB = 3cm, Bb = 2cm and bb = 1cm. The mean of these phenotypes is 2cm; if you
subtract this mean from each of the three phenotypes you get 1cm, 0cm and -1cm as the
difference. These values describe the additive effect of replacing one b allele with one B allele.
A single B allele has one half the effect of two B alleles, so our additive effect, a = 1. If we cross
a BB x bb we would get Bb with a beak size of 2cm. Crosses between these F1s would result in a
1:2:1 ratio of 3cm:2cm:1cm beaks and the mean of the F2's (2) would be the same as the mean of
the F1's and the mean of the two parents.
Now consider that BB and Bb have the same phenotype (i.e., there is dominance): BB = 3cm, Bb
= 3cm and bb = 1cm. A cross between BB and bb would produce Bb F1's all with 3cm beaks. An
F1 cross Bb x Bb would produce F2's with a 3:1 ratio of 3cm:1cm. In these the mean of the two
parents would be 2, the mean of the F1's would be 3 and the mean of the F2s would be 2.5.
Thus, dominance would affect the variation in phenotypes. There is a dominance component to
the variance. Thus the genetic variance can be partitioned into additive and dominance
components (and an interaction component which we will ignore, thank you): VG =
VA+VD+VI.
The total phenotypic variance is thus partitioned : VP = VA+ VD + VI + VE. The point of this is
that we want to know the additive genetic component of the total phenotypic variance since this
is what makes parent and offspring look alike and is what selection can act upon. We can thus
refine our description of heritability to mean the proportion of the total phenotypic variance that
is due to additive genetic effects: h
2
N = VA/VP where h
2
N means heritability in the "narrow"
sense.

Returning to our regression of offspring values vs. parent values (see figure 9.4 page 227),
the slope of this regression = h
2
N = VA/VP ( known as a midparent-offspring regression). This
allows us to define what kind ofresponse to selection we would get if we imposed a specific
intensity of selection on a phenotypic trait. The selection differential (S) is the difference
between the mean of the parents selected to produce the next generation and the mean of all
individuals in the population. The response to selection (R) is the change in the mean phenotype
after selection. The response to selection depends of the heritability of the trait:
R = h
2
N S (see figure 9.6 pg. 237).
An important consequence of this is that as selection proceeds, the additive genetic variation will
be reduced ("low" alleles removed). As the VA decreases, the heritability decreases (see equation
for heritability above). Will selection come to a halt?? Probably not because mutation is
constantly introducing a trickle of new alleles each with different additive effects. Under this
view the gradual changes in phenotype seen over long evolutionary times might be explained by
a continual mutation-selection balance. (see box 9.2 pg. 248).
What are the heritabilities of various traits in nature? They vary a lot (see figure 9.13, pg. 245).
One trend is that fitness-related traits tend to have lower heritabilities than other traits. Why? In
natural populations fitnesses determine our "selection differentials" so selection should remove
genetic variation for fitness traits and heritabilities will drop. Why then are not the heritabilities
of fitness related traits zero???? One answer: genetic correlations.
Due to the linkage of genes along chromosomes (or epistatic interactions among genes)
selection of one trait can lead to selection for another trait. If a viability gene is linked between
genes for bristle number, selection for high bristle number could lead to low viability if the low
viability allele became associated with the high oil content alleles. If this were the case, there
would b a negative genetic correlation between bristle number and viability. As it turns out,
many fitness related traits have negative genetic correlations (e.g., size of eggs negatively
correlated with number of eggs). Thus if fitness determines selection differential, selection in
natural populations could not remove all the additive genetic variation for two fitness traits that
are negatively correlated.



INFERRING PROCESS FROM PATTERN

The mechanics of population genetics attempts to describe how alleles and genotypes change
from one generation to the next. Often evolutionary biologists cannot study these transitions in
real time, either because the generation time is too long (redwoods, elephants) or the species are
fossils or other necessary information cannot be measured. In some cases the patterns of
variation can suggest or indicate what processes have been acting. Ideally we would want to
look at the patterns of variation and be able to say unequivocally that one or another process had
produced that pattern. This is not always possible since identical patterns can be produced by
very different processes. BUT: most patterns suggest obvious experiments that might tease apart
various processes contributing to those patterns.
Example: trajectory of allele frequency change shows a gradual but rough increase to fixation. If
we had this information alone we could not determine whether drift or selection drove the allele
to fixation. Design testable hypothesis to distinguish possible causes: measure effective
population size if pq/2Ne << p each generation might conclude selection drove allele
frequency change.
Biston betularia: pattern suggests selection; what is hypothesis and how would you test it? Bird
predation test: mark-release-recapture experiment in different areas: more dark preyed upon in
rural areas (see figure 5.5, pg. 108), more light form preyed upon in industrial areas. Patterns of
frequencies of dark form is very different in moths with different population structures. Biston
betularia has low density and flies far to find mates: frequency of dark form is quite uniform in
industrial areas. Gonodontis bidentata has higher density and is more localized: more variation
in frequency of melanic forms. Different balance of gene flow and selection. Two points: 1)
increased migration rate (m) leads to more homogenization of allele frequencies, 2) increases
effective population size (N
e
) means that selection will be more effective (weaker drift).
Heavy metal tolerance in plants. Selection inferred: mine populations have evolved resistance to
high concentrations of copper, zinc and lead. Test: for selection of genetic
basis: transplant plants across boundary and the "pasture" form cannot grow on the heavy metal
soil: implies true genetic response. Pattern of distribution: cline in frequency of resistant forms
as one moves across boundary. Suggests gene flow between tolerant and non-tolerant forms, but
despite gene flow divergence is maintained: must be strong selection to overcome effects of gene
flow. Examine patterns carefully: both the presence of a cline (frequency transition) and the
"steepness" of the cline can say thing about process.
Shell polymorphism in Cepaea nemoralis: find different colors (pink, yellow, brown) and
different banding pattern (five banded, two-banded, unbanded, etc.). Genetics worked out pretty
well: one locus for color, another for banding number and other modifier loci. Pattern: find
different morphs in different habitats. Is it selection or not? Hypothesis? = predation. Test=? look
at so called "thrush-anvils" stones where the song thrush who preys on the snails breaks them
open to eat. Look at the frequency of types of shells around thrush anvils and compare these
frequencies to the frequencies in the general population. Apparent that there is differential
predation by habitat: pink and unbanded snails more common in woods; yellow and banded
snails more common in fields and hedgerows. Implies that visual predation is important
character.
Allele frequency clines: Alcohol dehydrogenase locus (Adh) and o-glycero-phosphate
dehydrogenase locus (o-GPDH) have cline along the east coast of N. America. Hypothesis=?
selection differs with latitude. Test=? compare southern hemisphere: get same cline in opposite
direction implies selection but difficult to identify a specific mechanism
Leucine amino peptidase locus (Lap) in Mytilus edulis polymorphism varies with habitat and
position in Long Island Sound Lap94 allele found in higher salinity waters. Hypothesis=?
salinity. Test=? sample at different time of year with different runoff; find predicted results.
Physiology: determine how the different alleles work in the cell and differ in performance.
Results lead to a prediction of which should be in certain environments. Test prediction with
additional sampling. Test model of action of selection: phenotype could be additive,
mutliplicative or dominance. Each genetic model gives different fitnesses, hence predicts
different deviation from Hardy Weinberg genotype frequencies. Data fit predictions of one
model (dominance) well.

MOLECULAR EVOLUTION

For evolutionists the revolution in DNA technology has been a major advance. The reason is that
the very nature of DNA allows it to be used as a "document" of evolutionary history:
comparisons of the DNA sequences of various genes between different organisms can tell us a
lot about the relationships of organisms that cannot be correctly inferred from morphology. One
definite problem is that the DNA itself is a scattered and fragmentary "document" of history and
we have to beware of the effects of changes in the genome that can bias our picture of
organismal evolution.
Two general approaches to molecular evolution are to 1) use DNA to study the evolution of
organisms (such as population structure, geographic variation and systematics) and to 2) to use
different organisms to study the evolution of DNA. To the hard-core molecular evolutionist of
the latter type, organisms are just another source of DNA. Our general goal in all this is to
infer process from pattern and this applies to the processes of organismal evolution deduced
from patterns of DNA variation, and processes of molecular evolution inferred from the patterns
of variation in the DNA itself. An important issue is that there are processes of DNA
changewithin the genome that can alter the picture we infer about both organismal and DNA
evolution: the genome is fluid and some of the very processes that make genomes "fluid" are of
great interest to evolutionary biologists. Thus molecular evolution might be called the "natural
history of DNA". The points that follow are some interesting observations interspersed with
some basic concepts.
Some important background: DNA has many different roles in terms of function. Most of our
DNA does not code for proteins (more below) and thus is quite a different type of character/trait
than DNA that does code for protein. In eukaryotes, genes are frequently broken up
into exons (expressed) and introns (spliced out of the RNA before becoming a true messenger
RNA). The genes also have regulatory sequences that indicate when and where to transcribe the
DNA into RNA for protein synthesis. The genetic code is the information system for translating
the sequence of RNA into the sequence of amino acids. Within this triplet code some of the
nucleotide positions are silent or synonymous because any nucleotide in that position will do
(see table 2.1 pg. 25). This "universal" code is not completely universal because the
mitochondrial genome uses some of the codons in different ways (e.g., some termination codons
in the universal code specify amino acids in the mitochondrial code). Thus even the genetic code
can evolve.
Some important theoretical background: we want to develop a picture of what happens to a new
mutant in a population, lets say a single nucleotide change a one position in the DNA. This is the
starting point for molecular evolution. If the new mutant is governed by genetic drift, its fate
should be quite different than another nucleotide mutation that is governed by selection (see
below). To describe molecular evolution Kimura formulated theNeutral theory of molecular
evolution which is remarkably simple. If:
u = mutation rate / gene / generation, N = population size, then the number of new mutations
occurring per generation in a population = 2Nu (2 because we are considering diploid
organisms).
Now, when a new mutation occurs in a population its initial frequency = 1/2N because it is the
one new variant out of a total of 2N genes in the population. This is also its probability of
fixation because the probability of you reaching into a barrel of 2N marbles and getting the one
new marble is 1/2N. Thus taking these two values (the number of new mutations/generation and
the probability of fixation), the rate of substitution, K is just their product: 2Nu 1/2N =
u (substitution means that the new mutant goes to fixation in the population and substitutes the
original nucleotide or gene). Kimura got very famous for this simple bit of algebra. It tells us that
theneutral rate of molecular evolution is equal to the neutral mutation rate. Now a question
arises: what is the distribution of the types of mutations? Are most neutral? Are some
deleterious?; beneficial? (see figure 7.1, pg. 153 and box 7.2, pg. 176-177). One consequence of
the neutral theory is that genes with different mutation rates will have different rates of
evolution.
The rate of evolution of a gene or mutation that is under selection will be very different.
Similarly different genes with different functions, or different parts of a gene with different
functions will have different rates of evolution. Thus, different regions of DNA with
different functional constraints will evolve at different rates (see table 7.1, pg. 156; table 7.7,
pg. 183).
One prediction of the neutral theory is that silent (synonymous) sites in protein coding regions
will evolve faster than replacement (nonsynonymous) sites (due to different functional
constraints). This provides a null hypothesis about DNA evolution. Most sequences fit this
neutral model; however, the histocompatibility loci appear to deviate from a neutral model in
that there are more nonsynonymous substitutions than synonymous substitutions. This holds only
for the antigen binding region; the rest of the molecule is consistent with neutral expectations.
(see figure 7.10, pg. 185).
Another prediction of the neutral theory is that amount of sequence divergence will be
correlated with the level of heterozygosity; heterozygosity is measured as 2pq for a two allele
situation or (2pq+2pr+2qr) for a three allele situation, or 1- x
i
2
for i alleles; see figure 5.2 pg. 96
for a two allele view). Loci with high heterozygosity should evolve at a faster rate under the
assumption that these loci have a higher rate of neutral mutation (thus more variation within
species and more substitution between species; se Kimura's proof above). In general, loci fit this
relationship, however, balancing selection at a locus will introduce more heterozygosity then
expected. What about purifying selection?
Different rates of substitution have also been observed in different lineages of organisms: For
the human - chimp divergence, the rate = 1.3 x10
-9
substitutions/nucleotide site/year
for the human - Old World monkey split, the rate = 2.2x10
-9
substitution/site/year
for the mouse - rat split (=rodents), the rate = 7.9x10
-9
substitutions/site/year. Thus, rodents
appear to have a faster rate of molecular evolution. It has been argued that a shorter generation
time in rodents accounts for the faster rate of evolution, the so called generation time effect.
(see table 7.5, pg. 179). There are examples where short generation species have slower rates of
evolution; the point is that rates differ, the cause(s) of these rate differences have not been
unambiguously identified.
Most discussions of the rates of DNA evolution have been with respect to the molecular clock
hypothesis which states that there is a positive linear relationship between time since two
species diverged and amount of genetic divergence (e.g., DNA sequence difference) between
those species. These observations stated above indicate that there is not one molecular clock but
probably many molecular clocks that "tick" at different rates.
Lets say we identify a reliable molecular clock (e.g., number of amino acid substitutions in the
cytochrome C gene), we can use this to date, or corroborate, evolutionary events of interest (e.g.,
the divergence times for species that do not have good fossil data). For example: we know that
there are K
XY
substitutions between species X and Y and we know that they diverged T years ago
(from fossil data). Thus the rate of molecular evolution is r = K
XY
/2T. The denominator has a 2
in it because there are two paths of evolution on which the divergence can accumulate (ancestor
to X and ancestor to Y). Now lets say we obtain the sequence of cytochrome C from species A,
B and C (see figure below). From these data we count up the number of substitutions for all three
pairwise comparisons (the K's). We are given the date of divergence between A and C (=T1) and
we want to date the divergence of A and B (T2 = ?) but don't have any fossil data. If one assumes
that the rate of evolution is the same in species A, B and C as it was measured to be between
species X and Y, we can use the amount of sequence divergence between species A, B and C to
estimates their dates of divergence (measured in millions of years before present, MYBP). See
box 7.1, pg. 172.
Repetitive DNA Studies of many organisms has revealed that a large proportion of eukaryotic
genomes consists of repetitive DNA. Some of this is short localized repeats: in the kangaroo rat
the sequence (AAG) is repeated 2.4 billion times, the sequence (TTAGGG) is repeated
2.2 billion times and the sequence (ACACAGCGGG) is repeated 1.2 billion times. What it does
is unclear. Sequences like this have been called junk DNA. Note that junk is stuff you don't
throw away because it might be useful some day; garbage is stuff you don't want so you throw it
away. These sequences might have some function we don't know about so they have been called
junk DNA. The fact that such sequences seem to accumulate in genomes has lead to the notion
that repetitive DNA is selfish DNA, since the sequence makes additional copies of itself within
the genome decoupled from the reproduction rate of the host (i.e., the kangaroo rat).
Another form of repetitive DNA are transposable elements. These are sequences of DNA that
generally code for certain proteins and have the ability to move around the genome in a process
called transposition. There are quite a number of different types of such elements (we will not
review them all). The point is that they (like other repetitive DNA) are governed
by intragenomic dynamics as well as organismal population dynamics. An example is the P
element in Drosophila melanogaster. There are strains of flies that have P elements (P strains)
and strains that do not (M strains). When a P male is crossed to an M female the P elements enter
the genome of the offspring and jump around causing mutations (this is what we mean by a fluid
genome). A curious observation about P elements is that strains of flies collected from natural
populations before 1950 do not have P elements whereas flies collected from the wild after that
do have them. A variety of observations indicate that P elements invaded D.
melanogaster recently. The best evidence is that D. melanogaster's close relative do not have P
elements, but a more distantly related fly D. willistoni does have them and they differ by only a
few nucleotides over 2900 base pairs of DNA. These data suggest that P elements in D.
melanogasterare the result of a horizontal gene transfer (horizontal as opposed to "vertical" as
one inherits DNA from ones parents or ancestor "above"). Thus, not only can DNA move around
the fluid genome, but if DNA from one species can enter the gene pool of another without the
species fusing into one, one has to be very aware of what DNA sequence one is using to
determine phylogenies, etc.
If multiple copies of a DNA sequence are present in a genome we can think of each sequence as
a single "species" evolving on its own "line of descent" because each repeat will be mutated at
random. Thus if we had the complete DNA sequence of all the repeated P elements within a
genome, we would find that they are not identical and thus we could build a cladogram of these
elements much like we can build a cladogram of birds. When this sort of analysis was done on
different kinds of repeated elements (many copies of ribosomal DNA, for example) it was found
that the copies showed almost no variation. This observation suggested that all the repeats of this
family (ribosomal DNA family) were evolving in concert, i.e., together.
This pattern of homogeneity of repeats is called concerted evolution (figure 10.5, pg. 262). The
process(es) that generate this pattern could beunequal crossing over (see figure 10.2 & 10.6, pg.
258, 263) or gene conversion. Gene conversion is when the sequence of one region of DNA is
used as a "template" to "correct" or modify the sequence of another region of DNA. We do not
need to go into the molecular details of these processes, but that DNA can evolve in concert with
other sequences in the genome again indicates that intragenomic dynamics can influence the
pattern of DNA variation we see within and between species.
Gene duplication is a minimalist version of repetitive DNA (figures 10.1-10.3, pgs. 257-259).
Many genes in the genome are duplicated and when this happens one of the copies may be
"freed" from constraints and evolve a new function. The best understood case of this
phenomenon is the evolution of the globin genes myoglobin, o-hemoglobin, -hemoglobin. The
existence of duplicated genes forces us to recognize different kinds of homology because there
are two ways to have a common ancestor: by gene duplication and by speciation. When two
genes share a common ancestor due to a duplication event we call them paralogous (o-
hemoglobin and -hemoglobin in you are paralogous as are the o-hemoglobin in you and the -
hemoglobin in chimps). When two genes share a common ancestor due to a speciation event we
call them orthologous (o-hemoglobin in you and o-hemoglobin in chimps). Obviously when
constructing a cladogram from molecular data one should use orthologous genes if one wants to
build a tree of organisms.
A further example of the fluid genome is exon shuffling This is the pattern observed when exons
or functional domains of genes are shuffled together to form new or modified genes. Some
genes have very distinct domains that have clear relationships to other domains in very different
genes. It is thought that these domains have been moved around the genome by transposition or
illegitimate recombination events in evolution,accidentally forming new associations that happen
to have novel functions. Wally Gilbert proposed the idea of exon shuffling and argued that such
a phenomenon might accelerate evolution by creating new material for adaptive evolution.
One of the more interesting observations to ponder in molecular evolution is the C-value
paradox. The C value of a species is the Characteristic or Constant amount of DNA in
a haploid genome of that species. If we look at the diversity of organisms from viruses to humans
we see a clear trend in biological complexity. If we compare the C values across this range of
organisms (assuming viruses are "organisms") some of the less complex organisms have much
more DNA than the more complex organisms (see tables 10.2, 10.3, pgs. 259-260). This presents
a paradox. If DNA codes for proteins that give us form and function, what is a lowly alga doing
with all that DNA? We just don't know. Presumable most of it is not "functional" in the sense of
coding for proteins and RNAs. Much of it may be "junk DNA", but maybe this "junk" helps in
aligning chromosomes properly during mitosis an meiosis.
You now see why we referred to this topic as the natural history of DNA: these are "stories" we
know about how DNA "behaves" in evolution. The general point is that
the intragenomic dynamics of DNA and the intergenomic (interorganism) dynamics can be
radically different, but the patterns of variation we see in the current day are the summed effects
of both processes. This means we have to know some things about a piece of DNA before we
can use it as an evolutionary tool.



FITNESS AND ADAPTATION. I

General observation: most organisms show "good fit" to their environment. Desert
plants (desiccation resistant), marine organisms (fusiform body), cryptic insects All generally
can be placed in the context of the environment presenting a problem and the organism, through
evolutionary changes, providing a solution to the problem posed by the environment. The
apparent "good fit" between organism and environment suggests that this state increases the
survivorship and/or reproduction of the organism.
This may lead us to identify certain problems posed by the environment and ask how well does
the organism solve the problem Leads to a design/engineering approach to defining survival
ability, design fitness or engineering fitness. We do this by comparing form and function; often
there is an "appealing" match or sense of "fit"-ness. Is this what we mean by fitness
We then ask if the design/solution is the optimal solution suggesting an absolute engineering
fitness scale where the trait/attribute is assessed with respect to an ideal solution to the problem.
Alternatively, comparingdifferent available solutions may be all that matters: a relative
engineering fitness
This can be difficult because we could almost always "design" a system or part of an organism
with a slight improvement over what it has achieved by evolution. Does the presence of a design
that "appears" to have room for improvement mean that it is not "fit" Need to be aware of
the design constraints of organisms before making useful/contributory statement about level of
engineering fitness.
Darwinian fitness is assessed not by looking at the "fit" between form and function, but by
attempting to determine the contribution to future generations. What about grandchildless
mutants in Drosophila: have normal number of offspring, but these offspring are sterile. How
many generations ahead do we need to look? Since we can never really look ahead can we
really identify fit individuals/genotypes?
Another old problem: is Darwinian fitness a tautology? (a statement that is true by virtue of its
logical form; needless repetition of an idea), e.g. my father is a man; Brown students are smart;
the water is wet. Natural selection was characterized by Huxley as "the survival of the fittest".
The allele with high fitness will increase; allele A has high fitness; thus allele A will increase in
frequency. The premise provides for no alternative outcome, therefore it is a useless theory.
Survival of the fittest; who are the fittest? those that survive. Thus it reduces to survival of the
survivors. Characterized as such this tell us nothing and cannot be predictive?.
How do we get out of this? Assign the predictive aspect to the term fitness. Distinguish
between realized vs. expected fitness. A population passes through a generation, look at
frequencies of genotype before and after transition, define fitnesses by changes in frequencies.
This approach to fitness can lead us into the tautology trap: fitness defined by those that survive
better (post hoc), but the change may not have been due to natural selection (e.g. drift).
With true Darwinian fitnesses we would be able to predict which genotype would survive
better (fitness values assigned to genotype "before" generation transition). The "fitter" genotype
would have an inherent tendency to out reproduce competing genotypes.
G. C. Williams in Adaptation and Natural Selection, 1966, Princeton U. Press, states that the
problem "is not survival as such, but design for survival" (pg. 159). Thus overall "fitness" is a
combination of Darwinian and engineering fitnesses.
How do we measure fitness? Bacterial chemostats, one genotype increases at the expense of the
other. Fine if we believe that environments are ~constant over time (maybe they are in the
intestine) and that alleles with different fitnesses can be considered outside the context of the
entire genotype. Probably unrealistic for many haploids (and most diploids).
In diploids a bit more difficult: is it the phenotype, genotype or allele that determines fitness.
Well it is all: selection acts on phenotype which is produced by a genotype in a given
environment leading to the change in allele frequencies which in the next generation gives
different genotype frequencies. Problem: neither genotype or phenotype are inherited intact
(phenotypic "inheritance" depends on heritability of trait VG/VP )
One approach is to determine fitness of alleles e.g. "average excess" of allele:
p' = (p
2
w
AA
+ pqw
Aa
) / (p
2
w
AA
+ 2pqw
Aa
+ q
2
w
aa
) = [p (pw
AA
+ qw
Aa
)] / (p
2
w
AA
+ 2pqw
Aa
+
q
2
w
aa
)
where pw
AA
+ qw
Aa
= w
A
= fitness of A allele. Thus p' = p

Think about it: this is the frequency with which the A allele pairs with itself (the A
allele) resulting in fitness w
AA
plus the frequency with which the A allele pairs with the a
allele resulting in fitness w
Aa
relative to (i.e., divided by) the average fitness in the population
(wbar). This is a very nice formula since the ratio w
A
/wbar determines whether p will increase or
decrease in the next generation.

Fitness (selective) values of genotypes are a similar thing since they average the interaction
effects of the AA genotype over all other genotypes at all other loci in the genome for a given
environment: average fitness of AA when coupled with the B locus: (w
AA
= p
2
w
AABB
+
2pqw
AABb
+ q
2
w
AAbb
) assuming p=f(B) and q=f(b).
Note: selection will continue until: w
A
= wbar (i.e., the ratio is = 1.0 and p' = p(1), no change).
Thus average fitness in the population will be maximal but this does not mean the fitness of the
population is maximal.
Need to distinguish between individual fitness and population fitness. wbar is a description of
the average fitness of all individuals in the population. Does this determine the fitness of the
population? If we think of the population as the unit of "survival" a population with high fitness
is one that has a high tendency to out reproduce other populations. This is largely a demographic
question since drought, predators, parasites, etc. could alter a populations' probability of survival
irrespective of the number of individuals it is producing each generation.
A highly fit population is one that has a high reproductive output or is unlikely to go extinct.
These qualities can be unrelated to the average fitness in the population (although they can be
related).
Consider wasps living in nest holes. Population is limited by a fixed number of nest holes. Now
a mutation occurs that doubles the egg output of individuals carrying the mutation. Those
individuals with mutation are more fit, but the population will not increase due to limitation of
number of nest holes.
Consider prey switching in birds: mutation increases the fecundity of a moth. More caterpillars
present, birds switch their search image and prey more heavily on the abundant
caterpillars: reduces population size clearly the population is less fit.
These examples have assumed that population size is some measure of average fitness May not
be the case depending on the mode of selection: Soft versus hard selection. Soft selection is like
grading on a curve: there are always a certain number of As (or F's). Regardless of the absolute
fitness of individuals or the population the "better" ones will survive to fill those spots. Hard
selection assumes some threshold level of "fitness" that could be set by the environment. If all
individuals are below this level, population crashes; if all are above, population grows. See
figures 7.4, 7.5, pgs. 166 - 167) .


FITNESS AND ADAPTATION II

Adaptation is a central issue or concept in evolution, but one must be very specific when
defining or deciding that one is actually "looking at" an adaptation or that something is adapted.
The issue revolves around the general belief that the environment presents problems for the
organism and that adaptations provide solutions to these problems.
First: clarify some terminology. Adaptation come from ad (to, towards) and aptus (a fit). But it is
important to distinguish different uses of the word "adaptation" in the biological sciences. An
adaptation in physiology is a change in response to a certain problem: you heat up and respond
by taking off your jacket (a behavioral "adaptation" to an environmental problem); you continue
to heat up and respond by sweating (a physiologicalresponse to an environmental problem).
In an evolutionary context: also a change in response to a certain problem. This time the change
is genetic, is achieved by the process of natural selection and takes place over a period of time
considerably longer than the physiological time scale. But note: the physiological response itself
could be an "adaptation" in the evolutionary sense: it can be (is) adaptive (genetically)
to adapt physiologically or behaviorally.
The word Adaptation is both a state of being (phenotypic trait or character) and it is a
process by which such traits come to be called "adaptations".
Implicit in the term adaptation is the belief that an adaptation serves some function or purpose.
Dispersal and reproduction are the function or purpose of an apple, and apples are an adaptation
apple trees use to achieve reproduction. This assumes natural selection lead to the apple as the
agent of dispersal and reproduction. Avoiding predation is the function or purpose of leaf-like
coloration in katydids and preying mantids and their coloration is an adaptation these insects use
to avoid predation.
As argued by G. C. Williams it is important to distinguish adaptations from "effects": an
effect of being an apple is to provide food for insect larvae or humans; food is an effect of an
apple's phenotype (good resources); apple farming is and effect of apples' good taste and
nutritional value (apples did not evolve to solve the problem of providing work for apple
farmers); the cryptic coloration of a katydid is not for the purpose of demonstrating adaptation in
evolution lectures; demonstration is an effect of the striking morphology.
To reiterate: we identify traits as adaptations only when they evolved for the solutions of a
specific problem (function/purpose).
Selection is myopic: evolutionary trends are clear and presumably adaptive; some of these lead
to intensification other trends lead to diminution of characters. Examples: Elaborate secondary
sexual characteristics: increased horns, weapons in males displaying for
females; winglessness in insects: fleas adapted to reaching scalp/skin in hairy animals; eye
loss and reduced pigmentation in cave organisms: increase fitness by not shunting energy into
useless organs/tissues. All of these trends are adaptive but adaptation is not seeing the "goal" of
larger antlers or no eyes or smaller wings.
Now we have a problem of identifying adaptations in this context. Many traits evolved under one
selective regime and are now being used under a very different selective regime. The current
function may not reflect the context in which a trait evolved. We have to be able to distinguish
current utility from historical origin. Some traits may have evolved in one context but later
such a trait may be co-opted for use in a different role. One term used to refer to such traits
is Preadaptation. Some evolutionary biologists dislike this term (some get nauseous when they
hear it!) because the term implies that an adaptive trend was anticipating some future need. We
know that evolution is "blind", "shortsighted" and can't foresee or anticipate new selective
regimes. Key point is that a trait's function can change faster than its form.
S.J. Gould and E. Vrba (1982, Paleobiology vol 8 pg 4-15) have suggested a different
term: exaptation to stress the cooptedness of traits.
Three examples: the evolution of bone tissue is believed to have proceeded under selection for a
tissue that stores inorganic ions (e.g. phosphate ions). The ions need to be stored and released
depending on the physiological demands of the body. The tissue best at doing this became rigid
and could be coopted as a structural member. Thus organisms with "bone" as a structural tissue
entered a new "adaptive zone" and adapted for various functions. Skull sutures in mammals
appear as an adaptation for birth since they allow the skull to deform when passing through the
birth canal (a tight squeeze). But reptiles and birds have them and they hatch out of eggs. Sutures
evolved in one context (allow for growth of brain, head) but are an exaptation for birth in
mammals (they do allow for the head to change shape during birth which is adaptive). Isolating
mechanisms that prevent gene flow between incipient species. These evolved in allopatry prior
to any exposure to the sister taxon; isolating mechanisms may undergo subsequent adaptive
changes after being challenged by the related species. In all these cases the historical origin is
quite distinct from the current utility.
Exaptation also allows for the evolution of traits that originally had no "adaptive" function, but
later get coopted for a function.
The Adaptationist Program as it has been called by Gould and Lewontin (Section reading) seeks
to find adaptive explanations for every characteristic of the organism. Some things are not "for"
the "purpose" or "role" they seem to be filling (e.g. "Spandrels" [you must understand the
analogy of spandrels!]; read the paper!) some things are just nonadaptive and can be
distinguished from maladaptive (former = neutral; latter = bad). Think of your chin; it's not
"for" something, it is there due to differential growth rates of two growth fields (dentary and
maxillary) of your skull. Its just there. The striking pattern of white triangles on the Conus shell:
looks like it is "for" something but they live under the sand and mud and are not visible. Could
be due to chemistry of shell deposition or might have been "useful" in the shell's ancestor.
Notion of optimality needs to be considered in a historical context: again, consider current
utility vs. historical origin (see figure 13.5, pg. 351).
Another important point contra the Adaptationist Program is that some traits may not be capable
of achieving "maximal adaptedness" selection acts on the entire phenotype (debatable sensu units
of selection; later) andphenotypes are compromises. Orians' central place foraging model: bird
sits in middle of territory, may fly a certain route depending on availability and size of food
items. Could design and optimal foraging strategy BUT, when the birds leaves nest, young are
available for predation. Foraging strategy may not be the best foraging strategy, but the best
compromise given predation risk. Green sea turtle: excellent swimmer; terrible digger (not
designed for it) but must use flippers to dig hole for laying eggs. Flippers are not "optimal" for
digging, but they work.
Phenotypes as compromises underscores the importance of constraints. Evolution of one trait
can be constrained due to correlation among traits: selection for body weight in broiler
chickens: get more fat with it; selection for increase milk yield in cows: more milk (with higher
water content); selection for yield in soybeans: get less protein per bean; selection for nicotine
content in tobacco: tar content increases. These are artificial selection examples but can apply to
natural selection as well.
Constraints can be phylogenetic or developmental. (see figures 13.7, 13.8, pgs, 356-7; figure
13.11, pg. 361). It might be adaptive for certain mammals to be able to breath under water, but
their phylogenetic history and developmental program constrains them from evolving gills. They
"solve" this "problem" by tolerating high levels of lactic acid in their blood (and
other physiological adaptations of the diving response).
An informative means of analyzing adaptations is through the comparative approach. Wise to
put adaptations in a phylogenetic context example: rhinoceros horns. Experiments need to be
done to determine whether each unique pattern is uniquely adaptive or simply neutral variations
about a general adaptive theme (difficult experiments! can you design some?)
In seeking adaptive explanations for phenomena we should seek parsimonious adaptive
explanations: Flying fish goes out of water; how does it get back down. Physics offers a
parsimonious explanation; we could be adaptationist about it and say the fish evolved the means
of returning to water. Problem is not how it comes down, but why it takes so long to do so.
Gliding must be a result of natural selection. Point is: use the most efficient means to explain the
existence of a trait. G. C. Williams: Parsimony demands that we recognize adaptation at the level
necessitated by the facts and no higher.

LEVELS OF SELECTION

For natural selection to proceed there must be heritable variation in phenotypes and the
variation in phenotype must be associated with differential survival and/or reproduction, i.e.,
there must be differential fitness. By inference then, any entities exhibiting heritable variation
in rates of reproduction can evolve. We need not restrict our thinking to "individuals" in
"populations" in the traditional senses of these words.
Nature is organized in a hierarchical fashion. In terms of entities that can be heritable we can
consider genes, chromosomes, genomes, individuals, groups, demes, populations, species,
etc. Each of these entities meets the requirements of units that can be acted upon by selection. At
which level(s) does selection act? Answer: all of them. What then is the important unit of
selection? Answer: it depends.
First, some historical context. Serious consideration of a unit of selection other than the
individual was advanced by V. C. Wynne-Edwards (1962, Animal Dispersion in Relation to
Social Behavior). Populations have their own rates of origination and extinction and selection
could thus operate at the level of the group. Idea based on observation that many species tend to
curb their reproductive rate/output when population densities are high. This behavior would
favor groups that exhibited the behavior and select against those that did not; i.e., there would
be group selection.
G. C. Williams responded to this idea with Adaptation and Natural Selection (1966) arguing that
this behavior would be less fit than a cheating behavior where individuals did not reduce their
reproductive output at times of high density/low food availability. In general selection at the
level of the individual would be much stronger than selection at the level of groups. In keeping
with Williams' claim that one should always seek the simplest explanation for
selective/adaptive explanations, individual selection is usually sufficient to account for patterns.
Group selectionist thinking leads to statements such as "good for the species" when it is entirely
likely that it may be good for the individual as well: reduced reproductive effort in times of low
food may increase an individual's reproductive output at a later date.
Examples of selection at different hierarchical levels: Genic selection is selection at the gene
level; best example is meiotic drive (segregation distortion) where one gametic type (often one
chromosomal type) is transmitted into the gamete pool (or next generation) in excess (or
deficiency). The T locus in mice: affects tail length but also viability. TT homozygotes have
normal long tails; Tt heterozygotes have short tails and transmit ~ 90% of the t allele to their
sperm; tt homozygotes are sterile. Meiotic drive will increase frequency of t allele to point where
that become frequent enough to occur as tt homozygotes with appreciable frequency, whereupon
selection works against t alleles. Opposite Selection at two levels selection for at the level of the
gene; against at the level of the genotype (organism).
In this system the balance of opposing selection coefficients at different levels should give an
equilibrium allele frequency of 0.7 for f(t) allele (using data not provided here). In nature f(t) =
0.36. Discrepancy due to small local groups and drift. Some local breeding groups (2 - 4
individuals) fixed for the t allele and since tt is sterile, these demes go extinct reducing the f(t).
Thus we have selection at three levels: genic, individual and intergroup all contributing to the
maintenance of the t/T polymorphism.
Would we expect to detect meiotic drive systems in natural populations? If a new mutation arose
that introduced a bias in the transmission of the chromosome on which it was located, then it
would sweep to fixation and the locus would be homozygous for the "drive" allele. Meiotic drive
can only be detected in heterozygous state, so the drive system would disappear when the drive
allele went to fixation. There will be a window of time where the allele is increasing in
frequency, but this could be short-lived. If the drive allele reduced viability in the homozygous
state (as the T locus example), then variation can be maintained and the drive system would
persist longer, making it more likely to be detected.
Another case where genic selection may act: sex ratios. Why should the sex ratio be 1:1 in most
diploid species? Assume a sex ratio of 40% males and 60% females. Males in this case are in
limited supply. Any gene leading to the production of more males (a allele results in more males
the A allele at a sex determination locus) will be favored until the frequency of males is >50%.
Sex ratios tend to stabilize at 50:50 (R. A. Fisher, 1930).

Kin selection and altruistic behavior many species of animals that live in groups give warning
calls which alert other individuals about predators, etc. How could this behavior evolve when
making the call alerts the predator to the callers location and increases the possibility of the caller
becoming prey. Mammals that nurse their young: major energy investment for the mother may
be thought to reduce her fitness, but make obvious sense sine the individuals that benefit are
close relatives (offspring). Put in fitness terms: how could a trait evolve that lowers individual
fitness?
Key point is the term individual. If the ones that benefit from the behavior are related, the loss
in individual fitness may be regained in inclusive fitness, i.e., individual fitness plus fitnesses
of relatives. W. D. Hamilton argued that an altruistic trait could evolve if cost to altruist/benefit
to recipient < genetic relatedness (C/B < r) where r is an estimate of the probability of the donor
and recipient having allele identical by descent. For example parent - offspring have r=0.5;
siblings have r=0.5; grandparent-grandchild have r=0.25.
Idea of inclusive fitness implies that one's fitness is determined by one's own life time
reproductive output and the reproductive output of relatives, scaled by their degree of
relatedness (r). In the warning call example, if calling out to warn about the arrival of a hawk
killed you but saved three reproductively active siblings, it would have been worth it. If it only
saved two siblings, it probability wasn't worth it. Obviously one cannot tabulate the payoff of
event x, y, or z. The point is that the notion of inclusive fitness provides a fitness context where
altruistic behavior could evolve even when it appears to decrease individual fitness. Two modes
of selection: individual selection opposes altruism; selection among kin groups favors altruism.
Classic examples: helpers at the nest in birds. Young offspring remain at the nest to help their
parents produce more siblings in subsequent years/seasons. Helpers may contribute more to their
own fitness by aiding in the production of siblings than by trying to reproduce themselves and
failing due to lack of experience or availability of nest sites. Sterile workers in
hymenoptera (ants, bees, wasps): males are haploid (develop from unfertilized egg) so sisters
have r=0.75 because male contributes the same allele (relatedness between sibs
for paternal genes = 1.0; relatedness between sibs for maternal genes = 0.5; among diploid
female workers this averages out to r=0.75). A female worker does more to propagate her own
genes by staying in the nest and aiding in the production of sisters (r=0.75) than by going off and
producing her own daughters (r=0.5). Used as an explanation for the evolution of sociality
(e.g., colonies) in hymenoptera.
Group selection = variation in the rate of increase or extinction among groups as a function of
their genetic composition. Again consider how an altruistic trait could increase in
frequency. Differential rates of extinction: allele A confers altruistic behavior; at a selective
disadvantage to allele a within the group. Should lead to the reduction of allele A. But groups
with high frequency of A may be less likely to go extinct (due to better exploitation of
resources). Over all groups with high frequency of A persist and f(A) increases.
Differential productivity: similar to model above but altruistic trait affects reproductive
output of group. Selection against A allele within groups (selfish types have higher short term
fitness) but groups with high frequency of A exploit resources more prudently and actually
produce more offspring over the long term: f(A) increases. Model this as follows: assume
a haploid trait with A=altruist, a=selfish; p=f(A). In each population p decreases within a
population through time due to selfish individuals out competing altruistic individuals. But in all
populations as a whole the altruist gene increases over time. Below, the average f(A) across all
populations is 0.5 at the start:

Clearly, if this system were to continue for many generations, the frequency of the altruist gene
would decrease within each population. But under conditions where the selection favoring selfish
genes was weak and the group selection increasing the probability of staying extant (or the
growth rate of the population) was strong, and altruist allele might be preserved. Because the
conditions are so restrictive, group selection is presumed to be a rare phenomenon.
Group selection often involves plausible models but require that interdeme (group) selection be
strong. Would have to be very strong to overcome selection among individuals within
populations. Other complicating factors: turnover rate of individuals is faster than of
populations/groups; fixation of less fit allele is unstable to invasion by new mutant allele or
"selfish" allele introduced by gene flow. New research on multilevel selection suggests that there
should not be the necessary association between altruism and "sacrifice" or genetic "suicide".
Cooperation among individuals can actually result in higher group fitness without the assumed
loss of individual fitness (see a meeting review in Science (9 August 1996) vol 273:739-740). D.
S. Wilson makes the analogy between the optimal clutch size argument of D. Lack and the
optimal group of Wynne-Edwards. With too many eggs in a clutch an individual may die trying
to support them all, so some intermediate clutch size is "optimal" (see Life History Lecture).
Optimal groups may evolve intermediate density by the same trade-off mechanism.
A further problem for group selection: with localize population structure, there can be
considerable inbreeding which increases relatedness (r). Thus inter "group" selection that gives
the appearance of evolution of altruistic traits may be mediated by kin selection due to the high
relatedness among individuals.
Later we will consider species selection. Some lineages have more species than others, but are
these lineages more fit? Is this simply a pattern (more species) or is it really a different process?
Is it simple like bacteria in chemostats: a higher birth/death ratio; some lineages seem to speciate
faster than their members go extinct? Is this mediated at the level of the species, or can we
explain it (as G. C. Williams might like) at the level of individuals within populations?
Richard Dawkins likes to couch this discussion in terms of replicators and vehicles. Replicators
are any entities of which copies are made; selection will favor replicators with the highest
replication rate. Vehicles are survival machines: organisms are vehicles for replicators and
selection will favor vehicles that are better at propagating the replicators that reside within them.
There is a hierarchy of both replicators and vehicles. The key issues are that 1) the "unit" of
selection is one that is potentially immortal: organisms die, but their genes could be passed on
indefinitely. The heritability of a gene is greater than that of a chromosome is > that of a cell >
organism > and so on. But , because of linkage we should not think of individual genes as the
units; it is the stretch of chromosome upon which selection can select, given certain rates of
recombination. Issue 2) is that selection acts on phenotypes that are the product of the
replicators, not on the replicators themselves, but the vehicles have lower heritability and
immortality than replicators. What then is the unit of selection?? All of them, just of different
strengths and effects at different levels.

EVOLUTION OF BEHAVIOR

One general view in the study of the evolution of behavior is that behaviors can have a genetic
basis. This is not to say that all behaviors are genetically based; indeed many behaviors are
entirely culturally transmitted or learned and may have little to do with genetics (why are you
sitting in the same seat?). For genetically influenced behaviors we can treat them as we would
treat any other genetically controlled trait of an organism: 1) if there are genetically based
differences in a behavior, and 2) these differences affect fitness then, 3) behaviors can evolve by
natural selection.
Two examples of genetically based behaviors: cricket song. Different species of crickets have
different calling songs with different characteristics, e.g., inter chirp interval, pulse repetition
rate, etc. Hybrids between closely related species often exhibit songs with intermediate
characteristics (pulse repetition will be intermediate, inter pulse interval will be intermediate,
etc.) a hypothetical example with time on horizontal axis and each chirp = a group of vertical
lines:

Another example (on a larger phylogenetic scale) is head scratching with the hind leg in
amniotes (reptiles, birds, mammals; those with an amniotic sac). Most reach the hind leg over the
fore limb to scratch the head; that birds and mammals do it suggests that this behavior has a
genetically programmed basis and has been inherited through much of higher vertebrate
evolution.
Behavior is usually dissected into two components for analysis: Proximate causes/questions in
which one asks how the behavior is performed and ultimate causes/questions in which one
asks why the behavior is performed. Tinbergen has identified four questions to pose when
analyzing a behavior 1) what is the cause, 2) what is the development (ontogeny), 3) what is the
current function 4) what is the phylogenetic history. A strict course on evolution focuses more on
the latter two questions (recall adaptation/preadaptation/exaptation discussion and the
identification of current utility vs. historical origin).
Herring gulls breed is large colonies on the ground and defend territories. Two separate calls
used for 1) advertising nest site ("choking" call) and 2) as a territorial claim (the "oblique pose"
and "long call"). The Kittiwake also breeds in colonies but nests on vertical cliffs and its nest pad
is its territory and breeding site. In this species only one behavior serves both functions:
"choking" behavior is both defensive and part of mate recognition/pair formation. This is seen as
an adaptive behavioral shift wit respect to the nest location (steep cliff).
There are many behaviors that at first appearance do not seem "adaptive". Infanticide in
lions was first viewed as "aberrant" behavior by abnormal individuals because it was not "good
for the species" (male lions displace other males from groups of females and their offspring, and
frequently kill the cubs). It is true that killing infants is not, in the short term, an effective means
of increasing population numbers of a species. BUT, we now know (post W.D. Hamilton's 1963,
1964 papers on inclusive fitness and kin selection and G. C. Williams book on Adaptation and
Natural Selection) that the more appropriate way to address such problems is to think about them
in the context of whether the behavior is good for the individual.
In analyzing infanticide from the perspective of gene thinking it is 1) not adaptive for a male
lion to invest reproductive effort in an individual with whom he shares no genes and 2) once the
infant is killed it is advantageous for the female to come into estrous and have more offspring
with the new male (this will increase her reproductive output over leaving with the displaced
male, and not benefiting from other advantages of group living: foraging, avoiding predation on
young). Given the situation for both male and female, the observed behaviors make sense in
terms of propagating ones genes.
The role of the gene (or genes!) as the unit that is relevant in the evolution play an important part
in two influential books in the mid 1970s Sociobiology by E. O. Wilson, and The Selfish Gene
by Richard Dawkins. To grossly oversimplify one of their main messages: "an organism is just
DNAs way of making more DNA"
If we take the case of bird migration we want to know how the bird navigates to the breeding
location (solar and magnetic cues during flight), how the bird knows when to begin migration
(internal clocks and changes in day length [physiological changes]). There is usually a high cost
associated with migration so we also want to know why birds do it since many die in the process
(more time for feeding, more available food). Individuals that do migrate must leave more
offspring than those that do not - again gene thinking helps account for why the behavior exists
Population genetic approaches to the evolution of traits rarely tell us why a phenotype affects
fitness in a particular way; the models usually look at whether fitness increases or not.
The optimality approach to the analysis of behavior attempts to builds models where different
behaviors are treated as the traits and asks which one of these behaviors might evolve. The
approach generally ignores the mechanics of underlying genetic basis of the behavior (i.e., its
mendelian and transmission genetics). Optimal models assume there is a genetic basis and treat
each behavior as a haploid (asexual) trait that is inherited intact.
While Gould and Lewontin (and many others) have criticized optimal models, the builders of
optimal model (e.g., John Maynard-Smith, Univ. Sussex) argue that the models do not assume
that the organisms are optimal (because there are constraints on evolution of traits), but by
treating the problem as an optimality issue, it can tell you what kinds of
behaviors might evolve.
Two general type of optimal models: frequency independent models are designed independent
of what other strategies are doing, and seek to define the conditions which might influence
behavior (recall the "optimal foraging" model we described in the adaptation lecture where a bird
assess, quality, availability, distance to food items, etc.).
Frequency dependent models are ones where the strategy of one type depends on the strategies
and frequencies of other types in the population. The general approach is to look
for Evolutionary Stable Strategies (ESS) = a strategy that, if adopted by all, cannot be
"invaded" by a mutant strategy. Here a strategy = the behavior of an individual in a certain
situation. These types of model apply nicely to ritualized behaviors, distinct display behaviors
which take the place of aggressive interactions. Maynard-Smith's approach involves:
H = hawk who fights until the opponent retreats or will continue fighting injured with cost C
D = dove who displays but will retreat if the opponent escalates
V = payoff of winning an encounter
C = cost of losing an encounter
These values can be put into a payoff matrix:

In encounter with:


H D
Payoff to: H 1/2 (V-C) V

D 0 V/2

H:H interaction = 1/2(V-C) because each individual hawk will win half of the time and lose half
of the time. In the D:D interaction each will win half of the time and retreat half of the time
(retreat with no cost). Which strategy is an ESS? Answer by asking if a strategy can invade. Can
H invade a population of D's?: Is payoff (D against D) > payoff (H against D)? i.e., is V/2 > V?
Answer = NO, so H can invade a population of D's.
Is H an ESS? Is payoff (H against H) > payoff (D against H)? i.e., is 1/2(V-C) > 0? Answer: it
depends on the values of V and C: if V > C then payoff to H will be positive and H is an ESS; if
V < C then payoff to H will be negative and neither D nor H will be favored (H will always
invade a population of D's until H's become so frequent that they encounter each other
frequently. D can invade a population of H's because H's tend to damage each other too much. In
fact a population of all H's with V<C would go extinct. Thus which behavior evolves depends on
the nature of the interactions.
One can imagine many other games and payoff matrices that could be built to model other
behaviors. The point of all this is to imagine the following: some species have ritualized displays
that appear "civil" in an anthropomorphic sense. Have these behaviors evolved through a stage
where hawks killed each other (C was high) to their current state where the cost C to engaging in
a behavior is considerably less? This question could be addressed by comparing the behaviors of
related species and applying the game theory approach.

LIFE HISTORY EVOLUTION

For each organism a story can be told about how it makes a living. Most of the traits that are part
of this story have genetic bases and they contribute to fitness in some way. Usually in the
context of life history strategiesfitness is discussed in the context of different growth rates.
New mutations that alter the growth rate-related traits of organisms should lead to the evolution
of new life histories.
A few stories: the agave plant lives for many/several years in the harsh desert environment and
when sufficient rain occurs it sends up a tall reproductive structure, flowers, seets seed and dies.
The codfish after reaching sexual maturity may produce a million eggs in a reproduction, and do
so over several seasons; species of salmon forego reproduction until a late age, swim up current
in certain rivers/streams, sink all of their digestive tract and much of their muscle mass into eggs
in one reproductive effort, and die. Marine invertebrates: viviparous species have 20-100
offspring, primitive brooders have 100-1000 eggs/offspring, species with no parental
care have 1000-500,000,000 eggs (Aplesia, sea slug). How these different species achieve these
feats is one question (a physiological one). Why they do it is a very different one and difficult to
answer. We address this question by analyzing life history strategies.|
Best done by considering components of life history 1) survivorship and 2) reproduction.
Two further questions: 1) what is the best relative allocation of resources to each of these
components, 2) what is the besttiming of reproduction?
G. C. Williams suggested that there is a trade-off between survival and reproduction: if one puts
more resources into survival then there are fewer resources remaining for reproduction.
Conversely, reproduction is costlyand will reduce survivorship in subsequent years and reduce
the future reproductive output.

The bigger they get the more eggs they can produce. This presents a dilemma: when should they
reproduce?; now so they don't miss out?, later so they can produce more? but what if they get
killed? if they are going to die anyway why not now? how many eggs?, etc., etc. These are the
questions facing the existential poker player. One starts with a given number of chips (~ egg
yolk), how does one play one's cards? how does one invest one's chips (~ resources during
growth and development)? when does one decide to "fold" (wait until next year to reproduce
when the conditions might be better, new hand ~ random set of new environments)? what cards
do the other players hold (~ unknown variables of the biotic environment ~ competitive abilities
of the other "players").
All of these questions assume that the strategies have some high fitness solution. Lets
consider growth rate as one measure of a given genotype's (~ individual) fitness.
time 0 1 2... t
population size (at time t) N(0) N(1) N(2) N(t)
growth parameter

N(1) = N(0) => = N(1)/N(0); similarly N(t) = N(0)
t
=>
t
= N(t)/N(0)
This can be converted to an instantaneous growth rate using an exponential: N(t) = N(0)e
rt
where
r is comparable to . The point is that different genotypes could have different 's and hence
different fitnesses; selection = the difference between genotypes in their growth rates.

We can describe the net reproductive rate (Ro) of a genotype or individual in terms of its age
specific survivorship and fecundity: x = age, l
x
= probability of surviving from age 0 to age x,
m
x
= number of offspring produces by an individual of age x. Ro = l
x
m
x
= expected total
offspring per female during her lifetime. Now we can Calculate an l
x
m
x
table, or life table.
Age lx mx #offspr lx' mx' #offspr'
0 1 0 0 1 0 0
1 0.5 1 0.5 0.5 0 0
2 0.4 4 1.6 0.4 1 0.4
3 0.2 4 0.8 0.2 4 0.8
4 0.1 2 0.2 0.1 4 0.4
5 0 0 0 0 2 0

Ro = 3.1

Ro = 1.6
Note that the right hand column (a hypothetical new genotype called ') has the same l
x
schedule
and the same m
x
schedule except that it has been moved down one year (start reproducing later).
The genotype with theearlier age of first reproduction has the higher net reproductive rate.
This genotype will outcompete the other (') and selection acting on such strategies will have the
effect of reducing the age of first reproductionbecause those genotype with thes trait (early
reprod.) will have higher growth rate = fitness. This approach (l
x
m
x
) helps us identify those
components of a life history that might affect fitness and hence be selected for/against.
Charnov and Schaefer proposed a simple model to examine whether annuals (species living one
year) or perennials (species living more than one year) should be favored. P = number of
progeny that survive to reproduce (including the parent in the perennial case), B = number of
seeds produced, S1 = survival during first year of growth, S2 = survival during subsequent years
(subscript a = annual, p = perennial). for the annual: Pa = BaS1; for the perennial: Pp = BpS1+S2.
Now we wont to n=know when is Pa > Pp (i.e., when is the reproductive output of the annual
greater than that of the perennial?) Answer = when BaS1 > BpS1+S2. Rearrange to find that the
annual habit will be favored when Ba - Bp > S2/S1
In english this means that for the annual habit to be favored it has to have a reproductive output
greater than the perennial by the amount S2/S1 (i.e., the ratio of the "old" survivorship to the
"young" survivorship. The result fits well with observations about where annual and perennial
plants are found: many desert plants are annuals (low probability of survivorship), perennials
common in tropics).
Other issues that might affect the evolution of life history traits: Certain environments (arctic)
dramatic changes in weather/seasons can cause lots of death in a genotype independent
manner (in an extreme case). Selection that goes on might be more effective in the growth
phase after population crash; this would select for genotypes that have high rates of reproduction
(r), so-called r-selected species/genotype/traits (rapid development, early reproduction, small
body size, semelparity [reproduce once]). In more stable environments, where the population
might be near its maximum size, selection favors competitive ability to survive at the "carrying
capacity" (= K) of the population; such species/genotype/traits are said to be K-selected (slow
development, reduced resource requirement, delayed reproduction, large body
size, iteroparity [reproduce more than once]). This is best thought of a a continuum since
species are not either/or.
Another important way of thinking about life histories is bet hedging where variable
environments don't allow for the evolution of one particular strategy. Consider the evolution
of optimal clutch size ( how many eggs should I lay?). Again, the trade off between
survivorship and reproduction may determine one clutch size, but in a variable environment,
clutch sizes tend to be lower because there is an increased risk of losing an averageinvestment in
reproduction. A slightly smaller clutch can lead to a higher net reproductive rate (Ro)because it
can allow for more reproductive seasons than might be physiologically possible with larger
clutch sizes. This argument applies iteroparous organisms; the bet hedging in
a semelparous orgnanism might involve hedging on how long to wait before reproducing
because semelparous breeders will not have another clutch.

Other alternative strategies for dealing with spatial and temporal heterogeneity Dormancy (wait
out the bad times; seeds are good life history strategy here; an associated strategy is responding
to appropriate environmental cues for growth). Dispersal (spreading the risk in unpredictable
environments; fruits (carrying seeds) again good examples; aphids, crickets respond to
crowding by producing wings and dispersing.
The life table approach shows us that individuals of different ages are not "worth" the same in
terms of reproductive potential. A newborn at time 0 when population size = N(0) is 1/N(0) of
the population. In the next time interval the population has grown so a newborn is 1/N(0) of the
population and relative to a newborn at time 0, this newborn is "worth" =
(1/N(0))/(1/N(0)) =1/ = 1. Similarly a newborn born at time t is 1/N(0)
t
of the population
and relative to a newborn at time 0 it is "worth" = (1/N(0)
t
)/(1/N(0)) =1/
t
=
t
. Since the
population is growing, a newborn born at a later age is a smaller proportion of the
population. This means that older individuals contribute less to the makeup of the population.
Also, older individuals may be a smaller proportion of the pool of reproductive adults, so they
contribute even less to the population. The net effect is that the reproductive value of older
individuals is less than that of younger individuals. Reproductive value of an individual is
the contribution to future generations of an individual of age a. It can be quantified as
Va = (
a
/ l
a
)
x
l
x
m
x
Another way to think of this is the age distribution of test tubes in a lab:
more new one than old ones, associated with ageing is a finite probability of being broken, thus a
smaller proportion of all test tubes in the lab will be veery old. These old one will not contribute
much to "next generation"
Two points: 1) reproductive value may increase from birth to first reproduction (in species that
delay reproduction) because as one survives to this age, one increases the probability that one
will actually reproduce; 2) the drop in reproductive value with age can account for the evolution
of senescence (physiological decay with age).

Obviously genes for physiological decay would be selected against. But if ageing is due to the
expression of "decay" genes late in life, selection will not be able to act on them because the
genotypes which express this phenotype (decay) have very little reproductive value at that age.
Extreme example: a gene for death at age 80 could not be selected out of the population unless
individuals were reproductively active past this age. If you stop reproducing before age 80
selection will not result in differential survival of genotypes via phenotypic selection.

SEXUAL SELECTION

So far all of our discussions of selection have been without much regard for the sex of the
individual under selection (evolution of the sex ratio to 1:1 can occur through selection
for alleles in either males or females that favor the production of the rare sex). But just as with
natural selection individuals may differ in their ability to reproduce, in sexual selection there can
be differential reproductive success among individuals of the same sex (and species). In order to
mate, males need to gain access to females and vice versa, and not all individuals will be equally
successful at this task. If there are genetically based differences in the ability of one sex to insure
successful mating with the other sex, sexual selection will occur.
The patterns and processes of sexual selection are best understood in the context of parental
investment. Sexual selection occurs because there is a correlation between the gender of an
individual and its parental investment in each offspring. Parental investment is the investment
of resources that increases in the probability offspring will survive (a benefit) while decreasing
the parent's ability to produce more offspring (a cost). By investing in the production of current
offspring a parent will reduce the likelihood that it will be able to invest in future offspring.
Costs can be the energetic demands of parenting, increased predation risk, etc.
Parental investment should be proportional to:
(Benefit to current offspring survival) / (Cost to future offspring survival)

One important component of parental investment is the investment in gametes. This serves as
one means of distinguishing the sexes. Females are the sex with a large parental investment
per gamete. Example are eggs which have the nutrients to promote the development once
fertilization occurs. Males have a smaller parental investment per gamete; generally carries
only genetic information.
Some birds: each egg = 15-20% of a females body weight. In males, millions of sperm produced
each ejaculation; total output per reproductive season < 5% of body weight. (The difference is
less pronounced, but still significant, in mammals). This difference in investment in gametes has
important consequences for how these resources are invested and hence how selection might
act differently in the two sexes. In general, females should commit their eggs for
reproduction prudently; males need not be so cautious in their commitment of sperm. Put in
evolutionary terms, the reduction in fitness of a female that squanders an egg will be greater than
the reduction in fitness of a male that squanders a sperm (give or take a million).
Another important component of parental investment is parental care, care of the zygote after
fertilization. The amount of parental care is also frequently quite different in males and females.
In species with internal fertilization the female is "stuck" with the egg after fertilization. In
many species the female also cares for the young after they hatch. Males are not anatomically
tied to the egg and hence are sometimes "freed" from this additional parental care.
Moreover, in species where multiple matings occur, a male cannot be certain that a females
offspring were fathered by him. Benefit of caring for unrelated offspring is low, a male
can increase fitness by avoiding parental care.
General result is that sex with higher parental investment = limiting resource. Since this sex
is usually females, this will lead to male-male competition for access to mates (like resource
competition in ecology), andfemale choice where females choose among males so that they may
prudently commit their higher parental investment.
Put another way, males will increase fitness by increasing the number of fertilizations they can
perform, leads to Intrasexual selection (selection among individuals of the same sex). Females
will increase fitness by being choosy, leads to Intersexual selection where the high-investment
sex chooses among the low investment sex.
As a consequence, these forms of sexual selection can lead to the evolution of traits that better
enable each sex to perform its "fitness-increasing" behavior. In males: Horns, large body size,
sperm competition, mating plugs. In females: choosy behavior . The existence of choice in
females can lead to traits in males that tend to give individuals an advantage in attracting
mates: Plumes, coloration. These present a problem, however. Have these phenotypic characters
evolved so that males can out compete other males to gain access to females, OR, have they
evolved so that a male might win and the be in a position to be chosen by females? The relative
contributions of intra and intersexual selection in the evolution of some traits can be difficult to
distinguish.
Ecological contexts in which parental care might be given can influence the amount of parental
care invested in offspring.

For species in the lower left of the graph it doesn't pay either sex to invest in parental care;
species in the middle should exhibit sexual dimorphism (male showy, female less so or cryptic
to reduce predation risk); species at the upper right should both exhibit parental care,
monomorphic for plumage characteristics in birds
Evidence that the certainty an individual has regarding his/her paternity/maternity influences
the amount of parental care is available in fishes and amphibians. The table presents the numbr
of genera in each group (fish, amphibians) that fall into the categories.
Sex: Male Parental Care

Female Parental Care

Fertilization: Internal External Internal External
Group

Fishes 0 48 15 21
Amphibians 2 13 11 7
Internal fertilization: male cannot be sure that his sperm will fertilize the eggs in the female;
another male could come along and mate the female, displacing his sperm parental care does
not pay. With external fertilization a male can be quite certain that some of his sperm will
fertilize eggs so parental care does pay
Examples of sex role reversal: male has higher parental care, is the high investment sex and
should choose among females; females are the showy sex, males are the cryptic sex (another
bird example = phalaropes, female is showy). Difficulties of determining what is being chosen:
good genes?, good gifts? (wasp example) what is it about a male that will bring high fitness to
one's offspring?
Zahavi handicap model (a peacock's tail is a handicap because it may reduce fitness
by natural selection): females choose males with handicaps because males with handicaps must
have "good genes" in order to be exant while carrying the fitness-reducing handicap. Such a
system might evolve if the female's advantage by mating with the "good genes" of this male
outweighed the cost of her offspring having to carry this handicap around.
Kirkpatric model: flashy trait in male and the preference for it in female will become
associated (in technical terms, the alleles for the male's flashy trait and the alleles for females
choosing this trait come into linkage disequilibrium). Runaway sexual selection results which
can be non adaptive; sexual and natural selection can oppose one another.

EVOLUTION OF SEX

Why is there sex? We assume, anthropocentrically, that reproduction requires two individuals.
But in many organisms that is not true. Life originated without sex (as best we can tell) so sexual
reproduction is something that had to evolve.
First what is sexual reproduction? 1) production of haploid gametes by meiosis, a reduction
division, 2) fusion of these gametes produces a zygote and restores the full diploid complement
of chromosomes.
There are thus two parts to the evolution of sex: 1) the origin of sexual reproduction (cellular
evolution) and 2) the evolution and maintenance of sexual reproduction
and recombination (recombination is like sex in that it reassorts genetic material)
Recombination probably evolved ~ 3 billion years ago as a mechanism of DNA repair; sex
evolved ~ 1-2 billion years ago in the early eukaryotes; the reason is unclear but it its likely that
it is maintained in the current day by selection.
One "story" about the origin of sex is as follows (from J. Maynard-Smith, The Evolution of Sex,
Cambridge University Press, 1978):
1. Binary cell fusion (advantage ~ hybrid vigor; masking deleterious mutations)
2. Evolve the use of one spindle apparatus (advantage = maintaining both sets of chromosomes
and hence any hybrid vigor effects
3. Homologous pairing and chiasma (next step but advantage unclear; generates variation but
also creates regions of genetic homozygosity)
4. Reduction division + syngamy (favored to restore heterozygosity)
This may be one plausible scenario but why higher eukaryotes spend so much of the haploid-
diplod life cycle in the diploid stage is unclear
Subsequent evolution and maintenance of sex and recombination. Observation: one
can select (both up and down) for rates of recombination between two loci without
affecting other rates of recombination (see figure 8.6, pg.213). This means that there is genetic
variation affecting recombination, which in turn means that selection can alter the rates of
recombination.
The central problems with sex: 1) sex and recombination mix up any "coadaptation" that a
genotype might have to a particular environment; why disturb this if its is adaptive; 2) there is
a cost of meiosis associated with putting genes into males that cannot produce eggs. Consider the
following model: k = number of eggs, S = probability of survival, Parthenogenetic = unfertilized
eggs develop into females.

# adults # eggs adults next generation
Parthenogenetic females n kn Skn
sexual females N 1/2kN 1/2SkN
sexual males N 1/2kN 1/2SkN
Ratio Partheno/total n/(2N + n)

(Skn) / (SkN + Skn) =
n / (N + n)

If n is small, the parthenogenetic strain has effectively doubled in the next generation. This
assumes that the egg production by a sexual and a parthenogenetic female are same and that
the eggs of sexual females are equally divided between males and females. Why be sexual?
Advantage of sex in terms of genetic variation and rate of evolution. Consider two loci, A and B
and new mutations to alleles a and b which can interact to produce a genotype of high fitness in a
novel environment.. Since mutations are rare originally the only new chromosomes in the
population will be Ab (from a B -> b mutation ) and aB (from an A -> a mutation). An asexually
reproducing stain would have to wait for the second mutation because it has no way of
reassembling the existing alleles into new combinations. The sexual strain could produce the
high fitness genotype much faster by recombination (see figure 11.1 page 286).
This advantageous effect of recombination would be reduced in small populations because the
number of mutations occurring is the product of mutation rate and population size, so the
advantage of sex and recombination would be reduced in small populations.
These two observations suggest that sex might evolve by group selection: we have 1)
genetically isolated "groups" (sexual and parthenogenetic strains), 2) disadvantage to the
individual and 3) advantageous to the long-term survival of the group.
But G. C. Williams notes that the cases of facultative parthenogens (species that can reproduce
either parthenogenetically or sexually) strongly suggest that there must be some short-term
advantage to sex (otherwise it would be selected out of population as a strategy; note that we are
dealing with the same group here so the advantage of sex at the group level does not apply).
Some possible advantages:
Unpredictable environment theory: sex and recombination produces more genetically varied
offspring, individual using this strategy will have higher fitness since they have a high chance of
leaving an offspring that willsurvive in an unpredictable and changing environment.
Problems/qualifications: 1) if selection were sufficiently strong in the unpredictable
environment then there is a chance that the genetic variation produced by sex/recombination
might not be sufficient to "cover" the range of genotype needed. Considers the hard selection/soft
selection continuum
2) if there were continuous selection such that genetic variation was continually removed from
the population, there might be little variation remaining for sex to have an advantage.
3) theoretical models show that one needs to have the unpredictability be in the form of a switch
from hot-dry vs. cool-wet environments in one generation to hot-wet and cool-dry in the next
generation for recombination to really have a significant advantage.
Sib competition theory states that offspring in the next generation will be competing for the
same resources and thee genetically identical offspring will experience more severe competition
that sexual siblings because the latter will be genetically different and will not utilize resources
in identical manners. Supporting evidence from plants where offspring were shown to have
higher fitness when grown in competition with different genotype than in competition with its
own genotype.
Muller's ratchet and recombination. In a strain of asexual species the number of deleterious
mutations accumulate with time. The only way to get rid of them is by death. When the genotype
with the smallest number of mutations n
x
dies , the genotype with the smallest number of
mutations in now n
x+1
and thee "ratchet" has clicked up one notch. With recombination one can
mate two genotypes and their offspring might have fewer mutation (and more as well), so
variation is generated that can be a higher fitness than any of the existing genotypes.
The lower chromosome now has fewer deleterious mutations than
either parental chromosome.
Hitchhiking effect Deleterious alleles can become associated with advantageous alleles by
virtue of finite population size which will impose disequilibrium on loci (or association could
be due to lack of recombination and a deleterious mutation at an adjacent locus). Any other locus
which increases the rate of recombination will be favored because it will tend to break up the
association between the advantageous allele and the linked disadvantageous allele.
Converse of this is that any increase in fitness that occurs as a result of the interaction between
two loci, selection will act to reduce recombination because recombination would break up
favorable associations of alleles.
Parasites may also have played a role in the evolution of sex. Various data suggest that more
genetically diverse (heterozygous) organisms can mount a more effective defense against
parasites than homozygous hosts. Sexual reproduction might again have a short term advantage
in terms of sexually produced organisms having a greater defense system against parasites and
other infectious agents.

DEFINING SPECIES AND SPECIATION

While Darwin entitled his book "On the Origin of Species", the book dealt primarily with a
mechanism of evolution (natural selection) in which variation was critical. But what will
selection do with this variation? Change the frequency of dark morphs of moths, or morphs of
snow geese, or change the mean and the variance of the distribution of heights in human
populations? What is the result of disruptive selection? How do we decide that natural selection
has actually lead to the origin of new species? The answer to these questions depends on
one's species concept. The concept of species is an important but difficult one in biology, and is
sometimes referred to the "species problem". Some major species concepts are:
Typological (or Essentialist, Morphological, Phenetic) species concept. Typology is based on
morphology/phenotype. Stems from the Platonic "forms". Still applied in museum research (type
method) where a single specimen (type specimen) is the basis for defining the species. In
paleontology all you have is morphology: typology is practiced and species are defined
as morphospecies (e.g., snail shells in fossil beds). Problems: what about sexual dimorphism:
males and females might be assigned to different species. Geographic variants: different forms
viewed as different species? What about life stages: caterpillars and butterflies? If typology is let
run it can lead to oversplitting taxa: each variant is called a new species (Thomomys) pocket
gophers with > 200 subspecies.
Evolutionary species concept. "A species is a series of ancestor descendent populations passing
through time and space independent of other populations, each of which possesses its own
evolutionary tendencies and historical fate" (George Gaylord Simpson). Simpson was a
paleontologist and emphasis on stability over time is best appreciated in the fossil record.
Inherently morphological, but his claim is that morphologies have genetic bases, so it is
indirectly a genetical definition. Problem: gaps in the fossil record impose arbitrary boundaries
between species, especially those undergoing gradual size/shape evolution. Compare
with Cladistic species concept (pg. 418). How speciation affects existing taxa can alter one's
view of species.
Biological species concept. from population-level thinking of the modern synthesis.
"Species are groups of actually or potentially interbreeding populations which are reproductively
isolated from other such groups" (Ernst Mayr; Museum of Comparative Zoology, Harvard).
"Species are systems of populations; the gene exchange between these systems is limited or
prevented in nature by a reproductive isolating mechanism or several such mechanisms."
(Theodosius Dobzhansky; Rockefeller and Columbia Universities).
Not the first to claim the importance of reproductive continuity: "a set of individuals who give
rise through reproduction to new individuals similar to themselves" (John Ray, 1682). "A species
is a constant succession of similar individuals that can reproduce together." (George Louis
Buffon, 1707-1788). Note the characteristic Mayr: "biological" species concept implies that all
other species concepts are non-biological.
Recognition concept. species are groups of individuals that share a common fertilization system
(a "specific mate recognition system", SMRS of Hugh Paterson, South Africa). Emphasis is on
those characteristics of species that tend to hold them together; something that members of a
species share. Biological species concept stresses that which makes a species different from
other species; cant define species without reference to other species. Contrast isolation vs.
recognition. See figure 15.2, pg. 409.
There are other species concepts (now you know why it this has been called the 'species
problem'): Ecological, Pluralistic, etc. One philosophical approach is to ask whether species are
"individuals" or "classes".
There are some conceptual and practical problems with the Biological Species Concept: Are
species real or are they arbitrary categories imposed by biologists? Populations: where do they
begin and end; often arbitrary and grade into other populations; Genus, Family, Order, etc. are
these human constructs? Is a genus of bees = a genus of birds in terms of levels of organization?
What are the typological grounds for the boundaries. What about "species" that can freely mate
such as species of orchids that can mate sometimes between genera (wide cross). What
about asexual species? They don't reproduce with other species so every individual is a
species?? Mayr would hold that species are real units. Views species boundaries as being defined
by limits of gene exchange: each species is a group of populations held together by exchange of
genes in a genetic systemthat allows free recombination among the chromosomes of this system.
Holds that species are real objective units with definable limits - basic units of evolution. No
mistake that the Biological Species concept was advanced by two zoologists who worked with
organisms that did not present some of the more obvious problem of plants and bacteria
(Nevertheless, there is clear discontinuity in the phenotypes of bacteria).
Isolating "Mechanisms" (misleading term: is it a mechanism in that it evolved for the purpose
of isolating; or did isolating "mechanisms" evolve in one context and serve to prevent mating on
another?). Prematingmechanisms prevent interspecific crosses. Temporal or
Ecological isolation (don't meet due to different time of emergence or occur in different
habitats). Ethological (behavioral) isolation (meet but don't mate) e.g. fireflies. Mechanical
isolation (can't transfer sperm, morphological incompatibilities). See table 15.1, pg. 405.
Postmating isolating mechanisms inhibit or prevent interspecific crosses
gametic mortality (sperm transferred but does not fertilize eggs). zygote mortality (egg is
fertilized but zygote dies). hybrid inviability (F1 hybrid has reduced viability: incomplete
development). hybrid sterility (F1 hybrid viable but sterile) e.g., mule
Premating isolation prevents wasting of gametes: highly susceptible to improvement by natural
selection. Damselflies: character displacement of wing spot density. Rapid speciation events
often involve behavioral isolation: Hawaiian Drosophila: hundreds of species in the past several
million years. Postmating isolation does not prevent the wasting of gametes and its improvement
by natural selection is indirect. Isolating mechanisms may work in concert; if one breaks down,
another will prevent gene exchange (e.g., bird songs and plumage patterns). This issue of the
opportunity for selection to act on pre- vs. postmating isolating mechanisms is important in the
discussion of Reinforcement in the next lecture.
Breakdown of isolating mechanisms will lead to hybridization (crickets in eastern North
America hybridize in a hybrid zone along the Appalachian ridge). Are hybridizing "species"
really species? If the hybrids backcross to either type, introgression can occur ("the
incorporation of genes from one species into the gene pool of another species"). Many examples
of hybridization in both plants and animals. Often referred to as semispecies, i.e., not complete
species.
Population structure: are populations the unit of evolution? (Ehrlich and Raven 1969, Science
165:1288-1232) Species are just "phenetic clusters". But why do populations cluster into
"species". Checkerspot butterfly studied on Jasper Ridge near Stanford CA by Paul Ehrlich and
colleagues (1975 Science 188:221-228). Different populations fluctuate independently: suggests
little gene exchange between populations (But Slatkin's analysis of allele frequency data suggest
otherwise.
Geographic variation in reproductive isolation. If a series of populations can mate sequentially,
but the end populations cannot, is one species two?? Mayr would say that since they do not meet
the issue is not biologically relevant. Do you agree?
Polymorphism. Mimicry complexes of African swallowtail. Papilio dardanus exists as one
morph where no noxious species are found (Madagascar). Where noxious models are present the
same species (Papilio dardanus) takes on different forms depending on the local model; the
mimetic forms look like completely different species but are one.
Sibling species. Morphologically indistinguishable, but are reproductively isolated. Not always
easy to test for reproductive isolation and no morphological grounds on which to separate
populations.
Descriptions of the geography of population location/overlap helps focus on
how geography might influence gene flow. If gene exchange between two populations is
completely stopped, what will happen? Allopatricpopulations/species exist in different areas (do
not overlap or abut); sympatric populations/species occupy the same geographic
locality; parapatric populations/species have abutting but not overlapping ranges;
aperipatric distribution refers to peripheral isolates.

MODELS OF SPECIATION

Speciation is a fundamental issue in evolutionary biology, but it is both fascinating and
frustrating: we know it does happen but it its an historical phenomenon so it is difficult to
observe. The two camps of evolutionary biologists best equipped to deal with speciation (in
terms of mechanism, population geneticists; in terms of time-frames, paleontologists) are both
incapable of "seeing" speciation except in very special situations. We must rely on strong
inference to properly understand speciation. This inference is in many cases very rigorous and
scientific although it is historical, i.e., requires an interpretation of what has gone on in the past.
Defining speciation depends on one's species concept. (Recall species concepts: typological,
evolutionary, biological, recognition). In its simplest form speciation is lineage splitting; the
resulting lineages are genetically isolated and ecologically distinct. This implies that
something intrinsic about the new lineages (an aspect of its biology, e.g., genetics) makes/keeps
them distinct. Speciation then must involve the evolution of intrinsic barriers to gene
exchange. Intrinsic barriers can related in many ways to extrinsic barriers to gene exchange
(abiotic factors limiting gene flow: rivers, isolated islands, glaciers). A variant of a species could
be adapted to live in a particular environment that is spatially distinct from other types of
environmental conditions; here an intrinsic component contributes to an extrinsic barrier. The
notion of the evolution of barriers to gene exchangeapplies to virtually all species concepts since
unlimited gene exchange between two populations/species would prevent the evolution of the
defining principles of a given species concept: 1) true typological differences must have a
genetic basis, 2) evolutionary lineages would not have their own "evolutionary tendencies" with
homogenization due to gene exchange, 3) reproductive isolation (either pre- or postmating)
would not be maintained with unlimited gene flow, and 4) mate recognition systems could not be
maintained as distinct with unlimited gene exchange.

Without the evolution of some intrinsic barrier to gene exchange, fusion of the two incipient
species would be one likely outcome (populations would blend back into one), or extinction of
one or the other lineages (one population out competed [at the individual level!] the diverged
sister population leaving only one population).
MODELS OF SPECIATION
There are may models which have been proposed that enable barriers to gene exchange to
evolve; as argued by Ernst Mayr, geographic isolation provides the most effective barrier. We
thus consider the allopatric model:
1. continuous distribution split into two (or more) sub populations
2. differentiation in allopatry (different selection regimes; not necessarily selection for
speciation)
3. if populations come into secondary contact, no gene flow (= speciation complete)


If no gene flow after secondary contact, speciation was completed in allopatry. Speciation
would then be viewed as a byproduct of divergence in allopatry. What happens after
secondary contact is a matter of great debate: If the two differentiated forms mix
or hybridize this may provide the context for selection for assortative mating also
called reinforcement of premating isolation (reinforcement hypothesis). In this case speciation
was not completed in allopatry and fate of the two populations depends on the outcome of the
interaction upon secondary contact.
Patterns predicted from the action of reinforcement:

Selection in zone of overlap for increased premating isolation. See artificial demonstration with a
selection experiment (fig. 16.4, pg. 432).
Reinforcement model assumes that hybrids are less fit (=means by which selection for further
isolation can operate). This assumes that post mating barriers arise first and that premating
barriers arise as a result of selection in sympatry; these assumptions may not hold in all cases.
However, if premating barriers evolved first, there might be little hybridization (speciation
complete?); if there was no postmating barrier, even with small amounts of hybridization the two
forms would fuse back together because there would be no selection against hybrids!
Reinforcement is actually a special case of character displacement which is the accentuation of
differences between species (or forms) by selection against the individuals of similar phenotype
(reinforcement = reproductive character displacement and is achieved by selection against
hybrids). If reinforcement is true, we should expect to see displacement of characters associated
with pre-mating barriers to gene exchange in areas of secondary contact. Some cases we
do: calling songs of anurans; Frequently such reproductive character displacement is not
observed. When "reinforcement-like" patterns are observed, one has to be sure that the
phenotypic shift is actually an evolutionary response to the presence of the other incipient
species and not to some other clinal variation (e.g., ecological factors that generate parallel
clines).
Problems with reinforcement: other possible outcomes: fusion of the two populations because
differentiation was sufficiently slight that selection against hybrids is weak relative to the gene
flow between forms. extinction of one or the other of the two forms. Quite likely when there is
selection against heterozygotes. In population genetic terms, equivalent to heterozygote
disadvantage AA, Aa, aa with fitnesses 1,1-s,1, a metastable equilibrium

Selection against hybrids within the zone of secondary contact only favors displacement in
sympatry; gene flow in from allopatry will swamp the effect. One could view such hybrid zones
as genetic canyons of lost alleles. Another important question: if selection against hybrids is the
driving force for reproductive character displacement, how will the genes for the different
components of isolation/recognition sweep through the allopatric regions of the two species
ranges where there is no hybridization, hence no selection?
Another allopatric model is the Peripatric model referring to populations surrounding the main
part of the current species range. See fig. 16.5, pg 434.

1. Small isolated populations
2. Genetic drift via population bottleneck or founder event => new allele frequencies
3. new "genetic environment" => different response to selection than in main population
4. effect is a major genetic change = "genetic revolution"

One consequence is that speciation may not be dichotomous. Important consequence: rapid
divergence, unlikely to leave fossil intermediates (these possibilities will come in to play when
we discuss "punctuated equilibrium" later).
A variant on this theme proposed by Hampton Carson an influential evolutionary biologist from
the University of Hawaii is Founder-Flush speciation :
1. population initiated with small number of individuals (founders)
2. flush in population size; relaxed selection during this phase; low fitness recombinants survive
3. crash in population size; selection and drift determine which genotypes survive.

Carson's view: two "parts" to the genome: the "open variability system" and the
"closed variability system" Open system has much variability, responds rapidly
to selection (loci encoding allozyme polymorphisms such as enzymes in glycolysis and Krebs
cycle, etc.); closed system is resistant to selection; less variable ) loci encoding courtship song,
developmental patterns, etc.) In Carson's view the closed system is reorganizedduring the flush-
crash cycles, leads to a genetic change that contributes to reproductive isolation/mate
recognition.
Questions about the founder flush speciation: how small is population after crash?, how
long does population stay at reduced population size? Could retain a large portion of the genetic
variation after one crash; extended bottle necks will be more effective in reducing variation.
These questions also could apply to Mayr's peripatric speciation model
Parapatric Model of speciation. Ranges of two differentiated forms are contiguous and non-
overlapping. Patterns of discontinuities between differentiated forms/populations may be due to
secondary contact after a period in allopatry, or the discontinuity could be due to primary
differentiation in situ. One cause of this might be a steep environmental gradient or habitat
boundary (see fig. 16.3 pg. 428). With selection on loci that affect reproductive isolation/mate
recognition, populations can become differentiated. Will be apparent in the formation of a cline.
Can lead to sufficient divergence of reproductive/mating characteristics that barrier to gene flow
is established (e.g., plants growing on mine tailings have diverged in flowering time).

Studies of parapatric distributions are frequently concerned with the concordance of clines.
Selection acting on one locus/trait can impose a cline on another character if the two
characters/loci are linked. Are clines superimposed, shifted, different slopes. Slatkin (1973) has
shown that the width of a cline is: See fig. 16.9, page 439; text uses different letters
for equation). Different loci may have different cline shapes due to different strengths of
selection acting on them.
The text is a bit misleading about Parapatric speciation. It might lead one to believe that when a
hybrid zone is observed, parapatric speciation is involved. This is not true since the hybrid zone
may be the result of secondarycontact after allopatry, rather than primary differentiation at the
hybrid zone interface. Here again we need to determine the relative importance of the allopatric
phase and the parapatric interaction in determining the outcome of speciation (or fusion). The
cricket hybrid zone (fig. 16.8, page 438) is in fact the result of allopatry followed by secondary
contact (my personal knowledge), but Ridley does not let you know this.
Non-allopatric models of speciation are controversial but not impossible. Sympatric
speciation can be modeled with a two locus polymorphism, one locus (A) affecting fitness (in
this case by affecting fitness in terms of survival on one of two alternative hosts/patches), and
another locus (B) affecting mate choice which is crucial in the evolution of assortative mating,
a barrier to gene exchange (proposed by John Maynard-Smith in 1966)

AA Aa aa

BB Bb bb
host 1 1+s 1 1

mate w/ AA no preference mate w/ aa
host 2 1 1 1+t


These selective regimes maintain polymorphism at the A locus as in a multiple niche
polymorphism considered in the population genetics section. These sets of fitness/mating values
will result in the evolution of associations(e.g., linkage disequilibria) between the A and the B
locus (e.g., AABB individuals and aabb individuals will be found in the populations with few
intermediates.

these have high fitness these have low fitness
The green lacewings (Genus Chrysoperla; formerly Chrysopa) seem to exhibit patterns of host
preference and mate choice similar to that presented above (studied by the Taubers, Cornell
University). One form is adapted to one host/habitat and a second to another; this habitat
preference appears to be controlled by a single locus with other modifying loci (some
evolutionists have not accepted the lacewing data as conclusive).
See the other sympatric speciation model that involves variation in a resource base (fig. 16.10,
pg. 443). This model still requires the evolution of associations (e.g., linkage disequilibrium)
between fitness genes and behavior genes.
But, if sympatric speciation is, if not common, at least possible, is the model really sympatric?: is
it just microallopatric speciation (some argue NO if adults come up off their hosts into a
mating swarm, but then proceed to mate). Another crucial issue is: what is the rate of
recombination between these two types of loci since crossing over will break up favorable
associations. A model of host preference and assortative mating invoking many genes (polygenic
model) make it more difficult to maintain nonrandom associations. A general issue with all of
these models is how much gene flow is tolerated. Evolution of barriers to gene exchange is the
issue, gene flow = gene exchange; how much gene flow can take place and still evolve barriers
to the gene flow?? The answer depends on the genetic architecture of speciation (how many
genes, how much divergence, etc.; next lecture on genetics of speciation).
Saltatory speciation: Richard Goldschmitt in the Material Basis of Evolution proposed the idea
that Macromutations (mutations with big effects) would result in major developmental and
phenotypic changes in their carriers producing the so-called hopeful monster. Ridiculed at the
time; recently gained a new readership due to the molecular characterization of genes that cause
major phenotypic effects (more later on evolution of development). Big problem remains: who is
the hopeful monster going to mate with?
Chromosomal speciation: Consider a diploid with 2N = 4 chromosomes. If two such individuals
failed to undergo the reduction division of meiosis their gametes would be 2N=4. If these
gametes were used in fertilizationof one another, a new chromosomal number would be
established: 4N = 8. If this became stabilized as a new chromosomal type (and this is common in
plants), this new type can be reproductively isolated from the original 2N = 4 species. The
reproductive isolation would be due to an imbalance of chromosome sets in the new zygote: N =
2 gamete crossed to an N = 4 gamete results chromosomal type of 3N = 6. There can be two
consequences with this imbalance: i) inviability due to failure during development or ii)
instability during chromosome segregation could result in gametes with an incomplete set of
chromosomes (aneuploidy). These consequences could have the effect of a reproductive
barrier between the original 2N = 4 and the polyploid 4N = 8 type. Speciation can be nearly
instantaneous when such chromosomal events are involved (multiples of even numbered ploidy
levels: can produce gametes with some exceptions; multiples of odd numbered ploidy levels:
usually cannot produce gametes due to imbalance of haploid complements) => speciation.
Thus polyploid hybrids are frequency genetically isolated from their progenitors.
The simple inversion model (figure 16.17, pg. 457) illustrates another way that chromosomal
factors might play a role in speciation.
How should we think about speciation events? What are the models of divergence: is speciation
like a peak shift in an adaptive landscape, or is speciation a gradual divergence process on a flat
adaptive landscape? Main issue is whether the peak itself shifts and hence the population shifts
with it, or whether the two alternative peaks already exist and the problem is shifting between
the two alternatives.
Some fundamental issues in thinking about speciation: 1) does speciation require allopatry or
can speciation occur in non-allopatric contexts (sympatric, parapatric)?; 2) does speciation
require changes in many genes or can changes in a few specific genes lead to speciation?; 3) is
speciation itself adaptive or does speciation occur as a byproduct of adaptive responses to other
pressures?; 4) what determines the rates of speciation? (some lineages speciate at very different
rates).

GENETICS OF SPECIATION

Speciation has occurred, is occurring and will occur. These are undeniable facts. The problem
is: How do we study speciation? There is no single approach since there is no single mechanism
by which species speciate. Some approaches used in the past:
Study patterns of morphological change in the fossil record in a well defined lineage of
organisms. Success depends on many unknowns: stratigraphic resolution (will you "see" the
speciation event); distinguishinggeographic variants from true species (all you have is
morphology.
Comparisons of closely related species. These have speciated recently (assuming closely related
~ short time since speciation) so careful studies of their biology may identify important features
that contribute to reproductive isolation.
Study intraspecific variation. Look for evidence of incipient barriers to gene exchange. Perform
crosses between individuals from different regions; look for differences in genital morphology,
secondary sexual characteristics. These may show some bimodal distribution suggestive of early
steps in evolution. Must ask: what might we expect to find? This depends entirely on
the model of speciation that might apply to the organism under study. Looking within a large
species range for signs of variation may be fruitless if the speciation mode is peripatric with
genetic revolutions?
Laboratory populations might serve as model systems. One can establish the conditions of the
specific model under question and ask if the predicted divergence is observed. Mathematical
models can address specific predictions about modes of speciation. Both of these "artificial"
methods are important since they can identify what is possible. Knowing what's possible might
spur one on to looking for it in unexpected contexts in natural populations.
With the use of molecular tools the comparisons of intraspecific and interspecific genetic
variation has been studied in some detail. Aim is to identify genetic changes during speciation.
These data show us that genetic change is associated with speciation. We want to be able to
describe the genetics of speciation and the genetics of species differences. To do so we need
to distinguish genetic changes that cause speciation from those that accompany speciation.
These will differ a lot from one group of organisms to the next and will depend on the genetic
architecture of speciation. Best data on both of these issues have come from the many species
of Drosophila
Coyne and Orr (1989, Evolution vol. 43, pg. 362-381) take Ayala's approach one step further and
attempt to correlate genetic distance (Nei's D) with amounts of prezygotic and postzygotic
isolation. In the literature there are many reports of the amount of genetic distance between
closely related species of Drosophila and the amount of reproductive isolation between many of
the species for which genetic distance has been measured (premating or prezygotic isolation is
measured as [1-(proportion of heterotypic matings/proportion of homotypic matings)] which
ranges from - infinity for all heterotypic (between species) matings to 0 for random mating to +1
for all homotypic matings. Rarely do two species prefer to mate with the wrong type so the index
effectively ranges from 0 to 1).
Postzygotic or postmating isolation can be measured as in the following example. Consider
two species, A and B. These can be crossed two ways (reciprocally) to produce hybrid
offspring. We can also examine the viability or fertility of the two sexes of these hybrid
offspring, hence four contexts are examined to score postzygotic isolation:
Case Female parent Male parent Offspring Inviable or sterile?

1 Species A Species B Male No = 0 Yes = 1
2 Species A Species B Male No = 0 No = 0
3 Species B Species A Female No = 0 No = 0
4 Species B Species A Female No = 0 No = 0

I = 0 I = .25
Note: Isolation index is the average score for the four cases.
In any particular case one could choose to score isolation in terms of the presence or absence
of either isolation or sterility. Normally hybrid sterility evolves before hybrid inviability (mules
are sterile but viable). Hence an index based on sterility would have higher values than an index
based only on evidence for inviable hybrid offspring.
Coyne and Orr extracted these two types of data from the literature and tested some important
ideas about the genetics of speciation. The general idea is that genetic distance (D) is positively
related to time (the molecular clock hypothesis) and thus species pairs showing different
degrees of genetic distance should be at different degrees of completion of the speciation process
(be aware that many organisms are in the process of speciating as you read these notes). Coyne
and Orr show that there is a significant relationship between genetic distance and both premating
and postmating isolation
Two interesting additional points: sympatric species show greater prezygotic isolation than
allopatric species pairs. This pattern is consistent with the reinforcement hypothesis and suggest
that reinforcement can act (see figs. 16.14 - 16.16, pg. 454-455). A second observation: less
genetic distance between species pairs that produce sterile or inviable males than between
species pairs that produce sterile or inviable females(D
(A-B)sterile males
< D
(A-B)sterile females
).
This observation confirmed a well documented pattern known as Haldane's Rule (see table
15.2, pg. 406) stating that when hybrid crosses produce sterile or inviable offspring, the sex that
exhibits this is most likely theheterogametic sex (the sex with two different sex chromosomes,
e.g. X and Y in male humans and Drosophila; in birds and butterflies the female is heterogametic
with Z and W). Another "rule" of speciation is that genes affecting reproductive isolation are
typically found on the X chromosome (where X is the "female" chromosome; see another paper
by Coyne and Orr: "Two Rules of Speciation", in Speciation and its Consequences, 1989, D.
Otte & J. Endler, editors, Sinauer Associates).
The current belief about the large "X effect" is that advantageous mutations are more likely to
accumulate on the X since it is hemizygous in males, so half of the time recessive advantageous
mutations will be expressed. Similar mutations occurring on autosomes will be less likely to be
expressed because autosomes are always paired and an advantageous mutation would have to be
dominant to be "visible" to selection. Thus diverging populations (incipient species) will tend to
accumulate different mutations on their respective X chromosomes. When individuals are
crossed between these divergent populations, there will deleterious pleitropic interaction effects
between these new alleles on the X and other genes throughout the genome. The new mutations
certainly were not deleterious when they arose within each separated population, but when
paired with autosomes from a diverged population these mutations do not function properly, thus
one would only see the effect in a hybrid cross. See table 16.2, pg. 456.
Attempts to identify genes that keep species isolated go back to Dobzhansky in the 1930's:
crosses between D. pseudoobscura and D. persimilis produce sterile males and fertile females as
F1 hybrids. These F1 females can be backcrossed to males of either species, so the backcrossed
offspring can have all combinations of chromosomes. With four chromosome pairs in each
species, the F1 hybrid will have four heterokaryotypic pairsof chromosomes. The two possible
backcrosses (one in each direction) can result in 16 possible combinations of chromosomes.
Frequently find that the offspring with nonmotile sperm (= sterile) are the ones with sex
chromosomes from each species (see figures). Deleterious interactions between sex
chromosomes and/or between sex chromosomes and autosomes are implied, but the details are
the topic of a lot of current research (see Orr 1993, Nature vol. 361, pg. 532 & pg. 496). These
types of experiments, coupled with molecular biology may someday allow us to identify the
genes and the types of changes that can lead to speciation. Again, we would like to know
the genetic architecture of speciation: how many genes involved?; what sorts of mutations at
each gene? what sorts of interactions among genes? etc.

CASE HISTORIES OF SPECIATION I&II

Some of the best examples of speciation are examples of diversification on archipelagos. These
provide clear contexts of allopatry and hence provide the extrinsic barrier to gene exchange from
the source (usually mainland) population.
The most famous are the Galapagos Islands. The islands are young (some ~ 1 million years),
have a volcanic origin providing an opportunity for new arrivals to "radiate" into open niches and
the islands are quite distant from the mainland. This isolation and context of primary
succession (e.g., development of a flora and fauna on a "clean slate") will allow for a random
element in community composition. Irrespective of genetic consequences of the founding event,
subsequent evolution of species quite likely will be under dramatically different selective regime
than those in the source population.
Darwin's Finches. Morphological and genetic studies indicate that they are derived from single
ancestral finch, i.e., are monophyletic. There has been dramatic specialization in ecological
roles, each species having distinct morphologies and associated food items (beak size and shape
associated with seed size, grub feeding, tool use, etc.). Classic examples of different distributions
of beak depths: difference between means is greater between species when they occur on the
same island than when they occur alone on different islands (see figure below).
Often cited as a clear indication that competition played a role in the adaptive radiation of the
finches. There are obvious alternative hypotheses to explain these patterns: populations on
different island differ by these amounts as a consequence of drift; different islands have different
plants, insects (food items in general) thus the differences are a result of food, not competitors).
As P.R. Grant concludes in Ecology and Evolution of Darwin's Finches, Princeton Univ. Press,
1985, patterns of differentiation and speciation are a combined effect of adaptation to different
flora/food and adaptive responses to competitors. The issue of different plants/food on different
islands just shifts the question to another trophic level: how did the different islands come to be
different in these species.
Another evolutionary paradigm: the Hawaiian islands. Again the islands are young (< 5 million
years old), have a volcanic origin and an interesting one: convection currents in the earth's
mantle generate a "hot spot" where volcanic activity occurs above. The pacific plate moves
northwest over this spot so the islands' geographical location is related to their age (Kauai in
the north west is ~ 5 million years old; Hawaii [the big island] in the southeast is ~ 500,000 years
old and still active).
Hawaiian Drosophila show remarkable patterns of colonization and speciation. At least 700
species of Drosophilids on Hawaiian islands. Not just typical little fruit flies either: large body
size, dramatic "picture wing" species, some with "hammer-head" shaped heads. Banding patterns
of polytene chromosomes allows phylogeny reconstruction: these and other data show that
patterns of colonization are from older to younger islands (flies on Hawaii are derived from
ancestors on Maui). Most species are found only on one island (high levels of endemism; more
later in Biogeography). This implies that most new colonization events have lead to speciation
events! This observation lead Hampton Carson to propose the founder-flush model of speciation.
African cichlid fishes are another remarkable case of "explosive speciation" (the Hawaiian
Drosophila of the fish world). Geology and geography again plays an important role. African rift
lakes: great fresh-water lakes in east Africa. Formed recently: < 1 million years old. Lake
Victoria colonized by one (??) founder 200,000 years ago(??) now has ~ 200 species of fish!.
Recent study (Meyer et al. 1990, Nature vol. 347, pg. 550 and see pg. 512) used mitochondrial
DNA to show that the species in the lake are indeed monophyletic and that there is very little
sequence divergence between species: confirms short time span. But there has been remarkable
evolution of morphological, ecological and behavioral variation in these fish: algae
grazers, snail crushers, plankton feeders, paedophages (clamp onto the mouth of a fish
brooding her young in her mouth and force her to spit out here young into the mouth of the
attacker), one fish (in Lake Malawi) plucks the eyes out of other fish as food. All this diversity
in 200,000 years with very little genetic differentiation.
Another set of important examples of speciation are those that are believed to have speciated as a
result of isolation in Pleistocene refugia. Glacial advances and retreats during the Pleistocene
epoch acted as vicariance events in areas where glaciers were present (Wisconsin ice sheet).
Dramatic evidence of this is in the North American bird fauna and the clear faunal break between
the east and west, e.g., wood warblers; Peterson's field guides have an Eastern and Western
edition).
Climatic changes associated with the glacial advances and retreats altered habitats in the tropics
resulting in "islands" of habitat that fluctuated in size and geographic location, leading
to fragmentation of distributions and contribution to speciation. Believed to one explanation for
patterns of speciation in the Amazon. Also a possible explanation for the Larus ring species
complex: genus Larus (seagulls) fragmented in Siberia during the Pleistocene. Diverged
populations of Larus argentatus (herring gull) colonized eastern Siberia, across the Bering
straits, across North America, Iceland and back to Northern Europe becoming increasingly
diverged at each step. Hybrid zones exist between successive populations but the ends of the
ring are reproductively isolated implying that speciation has gone to completion (an example
of geographic speciation)
There have been some controversial examples of sympatric speciation documented in the
literature. The apple maggot fly (Rhagoletis pomonela) mates and lays eggs on a specific host,
originally Hawthorn. In 1864Rhagoletis was found on apple trees that had been introduced to
regions where hawthorn grew. In early 1960's Rhagoletis was found on cherry. This host race
formation has been argued as an incipient stage of sympatric speciation. Advantage of this
model is that the temporal framework is reasonably well documented and the species in question
is an agricultural pest so it is likely that it will receive further study and the issue can be settled.
Model invoking a survival locus (S) and a host selection locus (H) with each with new mutant
alleles that shift survival and selection to the new host (e.g., apple from Hawthorn).
Allochronic speciation was proposed as a model where species differentiated in time. Crickets
of the genus Gryllus were taken as an example because species with virtually identical songs and
morphology had evolved as spring adults versus fall adults (overwinter as juveniles or eggs,
respectively). The model may apply but this particular example was shot down by phylogenetic
analysis which showed that the two "allochronic species" (Gryllus veletis and Gryllus
pennsylvanicus are actually distantly related in the genus (see figures).

SCHOOLS OF SYSTEMATICS

First of three lectures on Systematics. We are following a natural progression from
the variation and dynamics of genes within populations, to divergence of populations
and speciation to systematics = the scientific study of the kinds and diversity of organisms and
their relationships.
A systematic or phylogenetic perspective on diversity of life itself follows logically from the fact
that there is a phylogenetic tree that relates all organisms: from one generation to the next there
is a pedigree that relates the parents to offspring. Within a population at any one time there is a
complex pedigree or network of the ancestry of genes that describes who received what genes
from whom. Among populations of a species there is a treeindicating which populations diverged
from others and the sequence of branching events of population separation. At the species level,
there is another tree of relationships that describes the sequence of branching events that led to
the formation of descendant from ancestral species. Thus, just as a kind of population
thinking is required to appreciate the evolutionary significance of variation among individuals, a
kind of tree thinking is required to appreciate the evolutionary significance of the history of
ancestor-descendant relationships that unites all levels of organization: genes, individuals,
populations, species, higher taxa.
What are the goals of modern systematics? 1. Differentiate individual organisms and establish
the basic units: species 2. to arrange these units in a logical hierarchy that permits easy and
simple recognition in the basis of similarity = classification 3. to keep the details of 1 and 2
separate = nomenclature 4. determine the evolutionary (ancestor-descendant) relationships
between all levels of the hierarchy =phylogeny.
Identification is not classification. Identification is to place an individual into an already
existing classification scheme. Classification is to assemble groups into larger groups. There are
conflicting goals of systematics:static classification of organisms into pigeon holes for easy
reference; but this should reflect a dynamic history of common descent = phylogeny. A
systematic solution to the problem of diversity incorporates both of these goals, but this result is
not always easily obtained.
Terminology: Taxon (taxa) = a group of organisms of any taxonomic rank that is sufficiently
distinct to be worthy of being assigned to a definite category. Category= rank or level in
hierarchic classification. Taxa = robin, thrushes, songbirds, birds, vertebrates, animals
Categories = species, family, suborder, class, subphylum, kingdom
How do you classify? Historically: Downward classification by logical division. Analogous to
"20 questions". In Aristotle's time things were either animals or plants. One could start by asking
oneself: is this an animal or a plant? Does this have feathers or not? and so on down until it was
properly placed in its category.
Linnaeus believed in the reality of the genus. He used downward classification through
his Linnaean hierarchy (kingdom, phylum, class, order, family, genus, species [recall: King
Philip Came Over From Germany Speaking]) to reach the genus and then make the final division
into the appropriate species. This approach lead to the Binomial nomenclature: Genus +
species: Homo sapiens, etc.
This methodology gave way to Upward classification by empirical grouping. It became
apparent that the groupings of Linnaeus were not Natural. The bottom of a downward
classification process often lead to groupings where members had clearly the wrong affinity.
Darwin's discovery forced the thinking towards Descent from a common ancestor. It became
apparent that these were the Natural groups that had been sought. What ultimately is the basis
for upward classification?Characters. Can take varied forms: morphology, chemistry, behavior,
ecology, physiology all could provide good characters.
Characters have character states: we all have hair, but our hair is different color; we all have
eyes but our eyes are different color. Character states may vary together in Character
complexes, or they may vary independently = Mosaic evolution of characters. Skin, eye and
hair color all vary together in humans. Is this three characters or one (pigmentation)?
Morphological and molecular characters may not evolve together, in a mosaic fashion (reading in
section next week). Different characters may suggest different patterns of relationships (see fig.
14.3, pg. 377), again an example of mosaic evolution.
Homologous characters = characters sharing a common genetic and developmental history.
Ancestor and descendant are linked by intermediate forms having the same character. These
characters are the basis of determining a true phylogeny
Analogous characters = homoplasious characters: two characters not sharing a common
genetic and developmental history and usually attained by adaptation to a similar ecological or
functional challenge. Bats and Birds forelimbs and wings: they are homologous as forelimbs,
but analogous as wings (a simple but crucial distinction).
Analogous characters are attained by convergent evolution where descendants resemble each
other more than they do their respective ancestors. Ichthyosaur, Fish, Porpoise; desert
plants. Parallel evolution e.g. marsupials (M) and placentals (P). Ancestors are viewed as
different but related. Point is: two possible evolutionary trees could be drawn:
(P,M) (P,M) (P,M) (P,M) or (M,M,M,M) (P,P,P,P)

If the characters that a set of organisms have could be either analogous or homologous
characters, the systematist is faced with several problems: 1) attempting to identify which are
which, and 2) deciding whether (or how) to perform character weighting. Excluding characters
is an extreme form of weighting (weight = 0). Placentals have a placenta, marsupials a pouch
where the immature young finish their development. These are major characters, should they
carry more weight in our assignment of relationship. If we looked for other characters in the
animals we could probably find many that would link the dog-dog, squirrel-squirrel, cat-cat,
anteater-anteater, etc. Since characters are the data we will use to do systematics other questions
arise: 1) should we use single or many characters?, 2) what are legitimate characters
(morphology, ecology, etc.)? 3) how do we weight those that are chosen?
Analogous/homologous problem revolves around the distinction of the similarity of characters
with adaptive or genetic bases. This leads to the distinction between grade and clade. Grade
= level of adaptation; organisms of similar grade due to similar adaptations due to convergence
(e.g., the "dog" grade or the "anteater" grade that goes across marsupial/placental
distinction). Clade = a group descended from one common ancestor; a genetic lineage (e.g., the
placental clade vs. the marsupial clade).
There are different schools of systematics: different schools place different emphasis on the
goals of systematics. Some will emphasize classification over phylogeny (grade over clade);
another emphasizes phylogeny over classification (clade over grade).
Phenetics (Numerical taxonomy) classification based on overall similarity of organisms. Treat
all characters of equal weight and amass as many character as you can. Enter the characters into
a computer that runs an algorithm that gives you a number reflecting the degree of similarity
between different taxa. Assumes: homologous and analogous characters will be in there together,
but rate of character change is roughly proportional to evolutionary distance and the homologous
characters will carry the day. Results plotted in a Phenogram showing evolutionary
relationships. See fig. 14.1, pg. 373, 14.4, pg. 378.
Cladistics (Phylogenetic systematics) Clade is everything. Define a hierarchical series of
dichotomous branching events reflecting ancestor-descendant relationships. Seeks to
identify monophyletic groups that, by definition, are derived from a single common ancestor.
Defines these groups as taxa sharing derived characters (synapomorphies). Assumes that
speciation is dichotomous producing two sister taxa and that the ancestral taxon disappears at
the speciation event. See handout for examples and terminology; see fig. 14.1, 14.2, 14.6, pg.
373, 376, 382.
Evolutionary systematics uses homologous characters but will commonly weight characters
differently depending on the "importance" of the character. A good evolutionary systematist is
one who "knows" the group and can thus decide which characters to weight more heavily.
Criticized as being highly subjective and not scientific because decisions are not testable
hypotheses, but statements of faith about the importance of the characters.
Acknowledges grade as relevant to the study: crocodiles and birds are different classes to
evolutionary systematists, but sister taxa to cladists.
Which approach do we use? Ideally a classification should be objective in that the criteria use to
classify are not subject to the whim of the person doing the classifying. Objectivity is important
if classification is to be a scientific endeavor: someone else ought to be able to step in and repeat
your "experiment" in classification. Moreover a classification should be natural and not artificial
so that if a set of characters were used to assign relationships, these relationships should also be
apparent in other characters not used in the analysis. There are natural groups that have been
generated during the history of life and systematists should attempt to discover these groups. In
recent years cladistics has become the dominant school of systematics as it meets these two
criteria well. However, phenetics is still very active and character weighting is still being used.
Note that natural groups might generate many more hierarchical levels than the classical
Linnaean hierarchy (see fig. 14.8, 14.9, pg. 386-387).
Terminology (See fig. 14.6, pg. 382 and note the different terms used for synapomorphy,
symplesiomorphy and that analogy = homoplasy).
Monophyletic - referring to a group of taxa descended from a single common ancestor (e. g.
angiosperms or seed plants)
Apomorphic - a derived character (seeds in angiosperms and gymnosperms relative to ferns)
Plesiomorphic - an ancestral character (stomata in angiosperms and gymnosperms)
note: apo and plesiomorphic are relative terms: vascular tissue is apomorphic to the
monophyletic group above the bryophytes, but plesiomorphic to the angiosperms)
Syn - shared Aut - "self", unique to a group
synapomorphies are shared derived characters and are what define monophyletic groups
because the members of that group have the character because they are descended from a
common ancestor (seeds in angiosperms and gymnosperms)
symplesiomorphies are shared ancestral characters (chlorophyll in the angiosperms and
gymnosperms)
autapomorphies are derived characters unique to one group (flowers in angiosperms)
autplesiomorphies can't exist, by definition
Paraphyletic group includes some but not all of the descendants of a common ancestor.
Incomplete grouping based on symplesiomorphies (e.g. the non-natural group of ferns and
gymnosperms based on the presence of chlorophyll and stomata; angios have these but are not in
the group)
Polarity distinguishes between the plesiomorphous and apomorphous state of a character by
comparison to an outgroup (a taxon know to lie outside the hierarchy of the groups being
considered, e.g., the outgroup algae determines the polarity of the evolution of seeds and
secondary growth with respect to the other taxa)
Sister taxa are the two lineages that descend from a common ancestor following a splitting
event; can be considered at any level of hierarchy in a cladogram

PHYLOGENETIC INFERENCE

The crucial issue in systematics is that there is a history of the organisms we wish to classify,
but we don't know that history. We must infer the sequence of branches or evolutionary
transformations that have taken place. There is a true phylogeny which we may never know, our
task is to collect and analyze data to provide the best estimate of the true phylogeny.
We will work some examples that illustrate the difficulty of this task. Phenetics: classification
based on overall similarity. See fig. 14.4, pg. 378. Matrix of shared character states. Those
taxa with the most number of similar character states are deemed more similar.
Distance (or similarity) matrix derived from morphological measurements, genetic distance
measures, etc. Each cell in the matrix is a value indicating the degree of difference (or similarity)
between the two taxa. These can be clustered by UPGMA (unweighted pair group methods with
averages). The two most similar (least distant) taxa are joined to form a group (e.g., taxa 1 & 2);
the length of each branch is half the distance value between the two taxa. The next most similar
taxon (3) is joined to the tree and the distance is calculated as the average of the distance from
taxon 1 to taxon 3 and taxon 2 to taxon 3. At each such step in building a tree, the number of taxa
in the matrix is reduced by one and new distance values are calculated as the average distance
from each member of the group just formed to each taxon outside that group. This process of
adding the most similar new taxon to a group is continued until all taxa are joined.
The tree produced is a Phenogram and is one way to infer relationships. Why might this tree not
reflect phylogeny (true ancestor descendant relationships)? 1) Variable evolutionary rates:
faster evolving taxon will be more different from all others and appear as an "outgroup"
2) Homoplasy (convergence) will tend to make character states similar between unrelated taxa
and the UPGMA approach will join them.
Cladistics: classification reflects sequence of branching events, not degree of
difference/similarity. See figures 17.6 and 17.7, pages 471-472. Classification is on shared
derived characters (synapomorphies). Note that relationships are never based on the absence
of characters (e.g., "Invertebrates" makes sense to us, but refrigerators and pizzas are
"invertebrates" because they don't have back bones, but they clearly are not related to animals.
For that matter, plants are invertebrates!). Tree produced is a Cladogram and is a hypothesis of
relationship. A taxon can evolve at a different rate, but it will tend to
accumulate autapomorphies which will not be shared with any other taxa and thus will affect
the branch pattern less (but variable rate can lead to incorrect cladograms). How
about Homoplasies? They will affect the hypothesis since those characters showing
convergences (or parallelisms) will contradict data from other characters.
This brings us to the topic of Parsimony: in constructing cladograms we seek that branching
pattern which requires the fewest number of evolutionary steps. Example of marine mammals
(chosen since we know that it is an example of a convergence). It is more parsimonious to evolve
fins twice and all the characters that hold mammals together once, than it is to evolve fins once
and all the characters that ally whales with other mammals twice. We tolerate fins
as Homoplasies (=analogies) since it is much more parsimonious than calling all the mammalian
characters homoplasies. See fig. 17.13, pg. 485 and work through it.
Parsimony is central to the cladistic method and can be used for both studying
the Polarity (direction of evolution in a transformation series) of characters and the confidence
of hypotheses of relationships. Example:Drosophila chromosome banding patterns (e.g.,
chromosomal inversions, figs. 17.16 and 17.17, pg. 491, 494). Each species has a distinct pattern
of bands in their salivary gland chromosomes. The sequence of bands appears to have
been inverted for certain sections of the chromosome during evolution. One can determine
a network of likely evolutionary steps from one species to another. Big problem: can start
anywhere in the network. Need to establish where the network begins, i.e. where to Root the
tree?
Choose an Outgroup: A taxon (or taxa) that are known to lie outside that group in question and
are thus believed to be ancestral to the ingroup. Requires independent information. Once
properly selected the determination of polarity falls out logically based on parsimony. the
identification of an outgroup can help identify Character reversals = reversal in a trend of
character change. An example is winglessness in insects: insects evolved from a wingless
myriapod ancestor, but there are groups derived (i.e., more recently evolved) insects that have
no wings (fleas). Wings have been lost in fleas and represent a character reversal. The use of an
outgroup is extremely important in phylogenetic inference as it allows you to determine
the "polarity" or direction of evolution as illustrated with insect wings. Once a reliable
phylogenetic tree has been produced based on a data set of characters properly rooted with an
outgroup, one can use the polarity provided by the outgroup to analyze the patterns of character
evolution in general (how many times does a character originate during evolution?). See fig.
17.9, pg. 476.
Another means of determining the direction of evolution in a transformation series is by
studying the development of the related taxa. Not as easy as "Ontogeny recapitulates phylogeny"
once claimed because different developmental stages can be lost either early and/or late in
development making difficult in some cases. In general, however, development can provide
resolving power in studies of transformation series (fig. 17.11, pg. 478).
Compatibility methods: go with the tree that is supported by the largest number of characters.
Said another way: the most likely tree is that which is supported by the greatest number of
independent characters (the largest "clique" of characters) in which there are no homoplasies.

MOLECULAR SYSTEMATICS

Molecular biology has revolutionized the field of systematics. DNA evolves by mutations being
incorporated in the DNA and fixed in populations. This will lead to divergence of DNA
sequences in different species. Although diverged, we can refer to two DNA sequences
as homologous (just as we would for any morphological trait such as forelimbs). Nicely
demonstrates descent with modification as a definition of evolution. For this reason, DNA
should be an excellent tool for inferring phylogenies: large number of homologous characters
that should be (??) less subject to convergent evolution than other characters that might lead to a
confusion of grade and clade.
To estimate phylogenies we first must estimate how much sequence divergence there has been
between the various taxa we want to study. Several methods: direct sequencing. Elegant
molecular methods available, a lot of work but provides lots of data. Each nucleotide position is
a character and the actual nucleotide that is present at that site is the character state.
A character can be phylogenetically informative when nucleotide changes are shared by two or
more taxa. A character can be phylogenetically uninformative when all nucleotides are the
same among taxa, or when only a single taxon has a different nucleotide.

I

U

I

A C T C G A C T A G A T
A C T C G T C T A G A T
A C A C G T C T A G A T
A C A C G T C T A C A T
A C A C G T C T A C A T

A less direct method of determining sequence divergence is by restriction enzyme mapping.
These are enzymes that recognize specific sequences in the DNA and cut the DNA strands.
Depending on the location of restriction recognition sites in the DNA, DNA fragments of
various lengths will be generated by the restriction enzyme digest resulting in a restriction
fragment pattern. One can also determine where various restriction enzymes cut a given piece
of DNA and draw up a restriction map of the stretch of DNA. The extent to which two
restriction maps (or restriction fragment patterns) are similar serves as an estimator of sequence
similarity (or difference). Restriction enzymes will recognize only a fraction of the entire DNA
sequence, so one will not know all the differences between two stretches of DNA. The data serve
as an estimate and because it usually involved less work can be done on many individuals.
DNA-DNA hybridization is another indirect way of obtaining estimates of DNA sequence
divergence between two taxa. DNA strands are melted apart at high temperature and allowed to
"reanneal" in the presence of the DNA of another species. One species' DNA has been labeled
with a radioactive nucleotide. This form heteroduplex DNA. The heteroduplex DNA is
gradually heated and the amount of single stranded DNA that has "melted" apart is determined
by the amount of radioactive label that is counted in each fraction collected from the various
temperature steps. Very similar DNA will melt at a high temperature and heteroduplexes
between diverged DNAs will melt at a lower temperature. Sequence divergence is proportional
to melting temperature. See fig. 17.19, pg. 497.
Phenetic approaches: DNA hybridization, sequence divergence from sequencing, restriction
patterns or restriction maps. In each case the data would be in the form of a single
number indication the similarity or difference between the DNAs of each pair of species in the
study.
Cladistic approaches: direct sequencing, restriction maps and restriction fragments (fragments
less desirable). In each case one would look for shared derived character states (nucleotide,
restriction recognition site) among taxa. With restriction sites shared loss is unreliable as a
uniting character because the nucleotide change could have occurred anywhere in the recognition
sequence. Like refrigerator/pizza/invertebrate example.
Molecular approaches to systematics for us to think about the rates of molecular evolution. If
DNA or proteins evolved at a constant rate in all species, then one could use estimates of
sequence divergence to build very reliable phylogenies. If there was a molecular clock we could
determine the "true phylogeny". Fact is, there is no one molecular clock.
Different proteins and DNA sequences evolve at different rates. Why? Different functional
constraints. Different proteins do different things and some can do their structural or functional
job with any of several different amino acids at many of the positions (fibrinopeptides). Other
proteins will not function properly with "any" amino acid changes (histones: two amino acid
differences between peas and cows!). Intron sequences less constrained than coding exon
sequences, and hence introns tend to diverge faster than exons. Synonymous sites evolve faster
than non-synonymous sites, again due to different functional constraints (i.e., some form of
selection against "incorrect" sequences). Nuclear DNA tends to evolve slower than
mitochondrial DNA (in vertebrates). Unit evolutionary period: time required to observe a given
unit of divergence. A 1% divergence of vertebrate mitochondrial DNA takes about 250,000 to
500,000 years.
What gene do I use??: Depends on the taxa you are studying and the amount of divergence
among them. Histones good for "macrosystematics", fibrinopeptides, mtDNA good for
"microsystematics" or population level phylogenies. See fig. 17.15, pg. 489.
Note problems with tree building from data: unequal rates and convergence.
As if the choice of gene/protein were not a problem. What if different lineages evolve at different
rates? Test for this with the relative rate test. Compare the paths from two different taxa to a
third taxon. If the paths are the same: taxa are evolving at the same rate; if not: different rates.
Extreme rate fluctuations are a problem; slight ones are not as they would not lead to regrouping
taxa (depending on how "slight" is defined)
Convergence over long stretches of DNA is unlikely, although it has been reported for lysozyme.
Another kind of "convergence" can occur due to the limited number of character states in
DNA. Back mutations: e.g. A changes to T, T changes to C and C changes back to A. Could
occur in one step or many. Maximal random divergence: 25% similarity
Nonetheless molecular tools have allowed major leaps in our understanding of biological
diversity: Bacterial evolution: three kingdoms, not five; Endosymbiont hypothesis, essentially
proven; AIDS virus: rapid evolution is good for the virus, bad for us.

COEVOLUTION

First some definitions: coevolution is a change in the genetic composition of one species (or
group) in response to a genetic change in another. More generally, the idea of some reciprocal
evolutionary change in interacting species is a strict definition of coevolution.
At first glance (or thought), it might seem that everything is involved in coevolution. This
assumption might stem from the fact that virtually all organisms interact with other organisms
and presumably influence their evolution in some way. But this assumption depends entirely on
ones definition of the term Coevolution.
The term is usually attributed to Ehrlich and Raven's study of butterflies on plants (1964) but the
term was used by others prior to 1964 and the idea was very present in the Origin of Species.
Ehrlich and Raven documented the association between species of butterflies and their host
plants noting that plants' secondary compounds (noxious compounds produced by the plant)
determined the usage of certain plants by butterflies. The implication was that the diversity of
plants and their "poisonous" secondary compounds contributed to the generation of diversity of
butterfly species.
Here we have a very general observation of one group of organisms having an influence on
another group of organisms. Is this coevolution? Some would argue that it is not good evidence
for coevolution because thereciprocal changes have not been documented clearly. Like the issue
of defining an adaptation, we should not invoke coevolution without reasonable evidence that the
traits in each species were a result of or evolved from the interaction between the two species.
Lets consider plants and insects: there is little evidence to determine whether plants' secondary
compounds arose for the purpose of preventing herbivores from eating plant tissue. Certain
plants may have produced certain compounds as waste products and herbivores attacked those
plants that they could digest. Parasites and hosts: when a parasite invades a host, it will
successfully invade those hosts whose defense traits it can circumvent because of the abilities it
caries at that time. Thus presence of a parasite on a host does not constitute evidence for
coevolution. These criticisms are quite distinct from the opportunity for coevolution once a
parasite has established itself on a host.
The main point is that any old interaction, symbiosis, mutualism, etc. is not synonymous with
coevolution. In one sense there has definitely been "evolution together" but whether this fits our
strict definition of coevolution needs to be determined by careful 1) observation, 2)
experimentation and 3) phylogenetic analysis.
The classic analogy is the coevolutionary arms race: a plant has chemical defenses, an insect
evolves the biochemistry to detoxify these compounds, the plant in turn evolves new defenses
that the insect in turn "needs" to further detoxify. At present the evidence for these types
of reciprocal adaptations is limited, but the suggestive evidence of plant animal interactions is
widespread. An important point is the relative timing of the evolution of the various traits that
appear to be part of the coevolution. If the presumed reciprocally induced, sequential traits
actually evolved in the plant (host) before the insect (parasite) became associated with it, we
should not call it coevolution. See different example figs. 22.6-22.7, pgs. 621-622 + text.
There are a variety of different modes of coevolution. In some cases coevolution is quite specific
such as those between two cellular functions. The endosymbiont theory proposes that current day
mitochondria and chloroplasts were once free-living unicellular individuals. These cells entered
the cytoplasm of other cells, an example of the general phenomenon of endosymbiosis. Current-
day mitochondrial and chloroplast genomes are much smaller than the genome sizes of their
presumed free-living ancestors. Some of this reduction in genome size is due to the transfer of
genes from organelle genomes to the nuclear genome. Thus, being in the cellular environment
has influenced the evolution of organelle genomes. There is evidence that the faster rate of
evolution of animal mitochondrial DNA has accelerated the rate of evolution of some of the
nuclear genes that function in the mitochondria. Thus there is some evidence
for reciprocal phenomena
Other modes of coevolution involve competitive interaction between two specific species.
The Plethodon salamander study is a good example: two species are competing: in the Great
Smoky mountains the two species compete strongly as evidenced by the fact that each species
will increase population size if the other is removed. Here there is a clear reciprocal interaction
between the two populations (species), each affecting the other.
[The role of competition between species, the coevolutionary responses to this competition and
the consequences for the evolution of communities is illustrated in the Anolis lizard fauna of the
Caribbean. There is coevolution because the competitive interactions between resident and
invading species of Anolis involve reciprocal responses in the evolution of body size. These
affect the structure of the lizard community as evidenced by the general pattern of there being a
single species of lizard on each island.]
Character displacement also provides and example of a pattern we might interpret as the result
of coevolution. Mud snails show pattern of character displacement in sympatry due presumably
to competition for food items (don't confuse this with reinforcement; the selective agent here
is not reduced hybrid fitness). We might call this co evolution because both species show a shift
when compared to allopatric samples of each species (mean of both ~ 3.2 in allopatry vs. ~ 4.0
and ~ 2.8 in sympatry). If only one species exhibited character displacement and you were a
really picky evolutionist you might not be convinced of a reciprocal response.
Another strong case is the Ant - Acacia mutualism. Here specific traits in each species appear to
have evolved in response to the interaction. The ant (Pseudomyrmex species) depends on
the Acacia plant for food andhousing; acacia depends on ant for protection from potential
herbivores (species that eat plant tissue). Specific characters of the plant appear to have
evolved for the maintenance of this mutualism: 1) swollen, ~ hollow thorns (= ant home), 2)
extra-floral nectaries (source of nectar outside the flower [i.e., the usual location] providing ants
with food), 3) leaflet tips = Beltian bodies (= 99% of solid food for larval/adult ants). Specific
characters in the ant that have evolved for the maintenance of this mutualism: 1) defense
against herbivores 2) removal of fungal spores from Beltian body break-point (prevents fungal
pathogens from invading plant tissues). The main point is that there are traits in both the ant and
the acacia that are traits not normally found in close relatives of each that are not involved in
similar mutualisms: mutualistic traits have evolved for the interaction in reciprocal fashion. See
another example : fig. 22.1 & table 22.1, pg. 611.
Coevolution may be considered among broad groups of taxa, so called diffuse coevolution (such
as the general coevolution between plants and insects [assuming it is real]). A nice idea, but in
fact the real action must be going on between pairs of species from each group. It is true that the
Pierid butterflies (family Pieridae) are associated with the plant family Cruciferae, so there may
be something general about each taxon that allows the coevolution to proceed. But the true
reciprocal events must be mediated at the host species-insect species level.
Mimicry presents a context were coevolutionary phenomena should be evident. Generally, we
would expect that Mullerian mimicry would be more likely to exhibit reciprocal evolutionary
patterns since both species involved are unpalatable and therefore have an opportunity to affect
the evolution of each other's color patters. This does not mean that Batesian mimicry (one
unpalatable model) will not involve coevolutionary phenomena, but the evolution of warning
coloration is certainly going to be more asymmetrical since the palatable species will show a
greater response to the state of the model than will the model show to the evolving state of the
mimic.
The Mullerian mimics Heliconius erato and H. melpomene. illustrate both the frequency
dependent nature of mimicry and the fact that each can influence the evolution of the other. One
would expect that the more abundant species would be the model in a mullerian system, since it
is what the selective agent (predation) is cueing on. In general H. erato is the more abundant of
the two species and H. melpomene mimics the wing patterns of H. erato. In one area of overlap
of the two species, H. melpomene is the more abundant and H. erato assumes the hindwing band
pattern of H. melpomene (see figure below). Thus depending on local conditions, both species
are influencing the adaptive responses of the other and thus fits strict definition of coevolution.
A crucial component of coevolution is phylogenetic analysis. If the cladograms of the host and
the cladograms of the parasite are congruent (e.g., figs. 22.2 - 22.3, pg. 612-613) this certainly
suggests coevolutionary phenomena. But again, be careful and think about it: cospeciation is just
"association by descent". Have there been reciprocal phenomena?; maybe just the speciation of
the host induced the speciation of the parasite and there was not parasite induced speciation of
the host. One needs to know the evolutionary history before we can make firm statements about
"co"evolution.

CONSERVATION GENETICS

Conservation biology is a rapidly growing discipline of cology and evolutionary biology. In
many ways the issues surrounding the conservation of endangered or threatened species have
rejuvenated aspects of population genetics and systematics that were often viewed as
"academic." Indeed, may aspects of conservation biology can be view as "applied" ecology and
evolutionary biology.
We will consider two different approaches to conservation genetics: 1) population genetic issues
relating to the maintenance of genetic variability, and 2) systematics issues relating to the
description of biodiversity and the recognition of evolutionary "units" for preservation.
Due to the rapid destruction of habitat there are many species that are going extinct. One
estimate is in the neighborhood of 100 species per day! Habitat destruction is generally
attributable to human impact, but the causes of extinction are varied: environmental variability,
natural catastrophes, demographic variability (stochasticity), genetic stochasticity, etc. Faced
with this problem, biologist set out to determine a Minimum Viable Population Size (MVP): a
population size that ensure the persistence of a species for specified period of time. One
description is a 99% chance of persistence of 1000 years.
Theoretical population genetics simulations have lead to some predictions. There should be a
positive relation between population carrying capacity (population size the (local) environment
can sustain) and the average time to population extinction. Moreover, extinction times are
exponentially distributed so a large proportion of populations will go extinct in a period of
time less than the mean time to extinction.

The implication from these simulation results is that Larger Populations are Better: it will take
longer for a larger population to go extinct, and larger populations will lower the extinction
curve. If environmental stochasticity is added to these models, theory suggests that MVP
should be 500 - 1000. If demographic stochasticity (randomly fluctuating birth and death rates,
i.e., random population growth rates), MVP needs to be sustained at higher values (1000 - 5000).
If this system is placed in the context of an interwoven ecosystem, the MVP should probably be
higher.
MVP and Genetic variation Population genetic theory indicates that inbreeding
depression will be likely with an effective population size of N
e
< 50. To avoid the possibility of
inbreeding, a lower limit of MVP = 500. These numbers may seem like obscure conclusions
from a series of complex Populus simulations, but they are the working numbers for policy
issues : N = 50 defines the critical list; N = 500 defines the endangered list.
The values for MVP and "critical" versus "endangered" lists stem from some basic issues
relating to effective population size. N
e
refers to the effective number of breeders in the
population, and can be affected greatly byvariance in reproductive success A focus here is the
ratio of effective size to census size N
e
/N ratio. Observations from field and laboratory
experiments indicate that N
e
/N ratios are about 0.25 (range = 0.05 to 1.0). This means that either
some individuals are breeding and others are not, or that some individuals have
different degrees reproductive success that others. It is possible that a substantial proportion of
the population does reproduce, but that a small number of individuals produce most of offspring
reducing the genetic pool from which alleles are drawn. This reduces the N
e
/N ratio and hence
brings the population closer to the demographic danger zone.
With a N
e
/N ratio of 0.25, the census size should be 4 times higher than the simple numbers
predicted by "critical" and "endangered" estimates. Now add population size fluctuations:
bottlenecks in census size affect N
e
more severely. Recall: = (1/N
e
) = (1/t) (1/N
e
)
The net effect of these factors is that MVP should be 5X to 10X N
e
.
Given a finite amount of space for a nature preserve, do you establish a Single Large or Several
Small (SLOSS) system. The answer depends on the likely causes of extinction in the particular
system of concern. If the species is subject to demographic fluctuations, it would be better to
maintain one large system, since the plot above suggests that extinction is more likely in small
populations. In systems of species where environmental stochasticity is a general problem , the
Several Small approach is probably better: many sub-reserves will reduce the chances of losing
the entire system.
The SLOSS debate is closely related to the dynamics of Metapopulations. The maintenance of
genetic diversity can be enhanced by structuring in a metapopulation system. Alleles that might
be lost in one deme can be fixed in another, and the average of the metapopulation system may
maintain more heterozygosity than a simple population of similar total population size. The
solution to this is not general since metapopulation systems may have varying degrees of
migration between demes (at some level of migration, metapopulations become 'systems of
subpopulations' since in the strict sense the demes of a metapopulation experience little gene
flow.)
Metapopulations can also contribute to the purging of deleterious recessive alleles. With some
level of inbreeding in demes, deleterious recessives will be selected against. With limited
amounts of gene flow, the system can effectively purge these alleles that might not be expressed
in a large random mating population. One approach is to have semi- isolated subpopulations
with corridors for dispersal.

There is no one solution to all these problems. The answers depend on 1) the species and
ecosystem in question, 2) the demographic issues (constant or variable) and 3) the existing levels
of genetic variation.
Many issues in conservation genetics have been centered around Zoo Biology. Most zoos
maintain rare or endangered species and are involved in captive breeding programs with such
species. Again, a central issue is the maintenance of genetic variation. A number of recent
studies have addressed the captive breeding protocol to determine how mating systems affect
the maintenance of genetic variation.
Using Drosophila, several studies have shown that populations maintained with equal founder
size (EFS) retain more genetic variation that populations maintained by random mating. EFS
approaches equalize the number of founders that contribute to the "captive" population each
generation. Similarly, equal founder representation (EFR) studies retain slightly more genetic
variation than randomly mating populations. EFR populations are maintained with a controlled
pedigree where the parentage of each contributing female and male is known. These types of
studies use allozyme electrophoresis to study directly the levels of heterozygosity in
experimental (EFS, EFR) and randomly mating control populations over time. In
addition, fitness studies can be performed by competing experimental flies against tester
stocks to determine if a higher fitness is maintained. The conclusion from these studies is that
controlled mating schemes can make a difference in retailing genetic variation and attaining
higher levels of fitness. The next step is how do you translate these findings into captive
breeding of Panda Bears??
Phylogenetic approaches to conservation biology have received a lot of attention. This follows
directly from the general concern about Biodiversity. To properly appreciate and understand
biodiversity, we must have a sense of phylogenetic structure of the taxa involved. This applies to
broad levels of organization (soil bacteria, plants, animals) as well as to smaller taxonomic units
(populations within species). Molecular systematicapproaches have been of great use since
many new techniques can be applied without harming wild individuals, and can even be applied
to museum skins for historical comparisons. In the context of the Endangered Species
Act several important issues come up: What is the phylogenetic relationship of the endangered
species? How much and what type of genetic variation (gene trees)? What do we preserve?
What IS a species? Any genetically distinct entity has evolutionary potential.
Two case studies: The Dusky seaside sparrow: The species declined in the 1960's; by 1980 only
6 birds remained that were all male. A captive breeding program was initiated and
captive Scott's seaside sparrow was chosen as the females. When the last male Dusky died
Avise & Nelson analyzed its mitochondrial DNA (mtDNA) and found that the Dusky and Scott's
seaside sparrows were members of different clades on the phylogeny of these sparrows. The
implication is that more detailed phylogenetic knowledge of the endangered species would have
lead to different management decisions in handling this captive breeding program (choosing a
different species to mate to the Dusky)
The red wolf was placed into a captive breeding program in 1974. By 1975 it was extinct in the
wild. Early data suggested that red wolves hybridized with coyotes. Since coyote populations do
well in human-disturbed habitats, hybridization may have affected the survival of the red wolf.
Wayne & Jenks studied the mitochondrial DNA from captive red wolves and from 77 animals
collected from the wild during the capture program. They also used the polymerase chain
reaction (PCR) to sequence mitochondrial DNA from museum skins ("ancient DNA techniques")
collected before hybridization between red wolves and coyotes is thought to have begun. They
found that red wolves have either a gray wolf or a coyote mtDNA, indicating that the red wolf
"species" is entirely a hybrid. Other researchers disagree about the species "status" of the red
wolf. Nevertheless, this raises the question: What should we protect? If the species isn't really a
clear entity phylogenetically, does it deserve a conservation/captive breeding effort? Wayne &
Jenks argue that their data should not be used to advocate the discontinuation of the conservation
effort of the red wolf.
These examples illustrate why the recognition of Evolutionarily Significant Units (ESU) is an
issue of great concern in conservation genetics. ESUs are defined various ways, but they are
recognized as populations with independent evolutionary histories. Fixed allelic differences or
strong phylogenetic support such as multiple synapomorphies distinguishing one population
from another are good grounds for the recognition of distinct ESUs. Hence, a full understanding
of how to do molecular systematics is very important in molecular conservation genetics.
It should be emphasized that mitochondrial DNA markers are maternally inherited and may not
reflect the true evolutionary history of the entire populations. Hence it is advisable to have
additional nuclear markers for ESU recognition such as allozymes, RAPDs or microsatellites.
RAPDs are Randomly Amplified Polymorphic DNA. This method uses the polymerase chain
reaction to amplify random regions of the genome with short random 10-base primers.
Microsatellites are regions of the genome that vary in the number of tandemly repeated
sequences. The repeats are short (2-4 base pair repeat unit), but there may be many of them in a
row. Individuals differ in the number of repeat units they have and this difference can be
determined by gel electrophoresis.
Another relevant level of concern is a Management Unit (MU). These are defined as
populations that have different frequencies of alleles, but do not necessarily
show fixed differences between populations. Hence several MUs may exist within an ESU. The
figures below illustrate the difference. The general lesson is that molecular approaches to
conservation biology are potentially highly informative since many overt phenotypic
characteristics cannot reveal important differences that distinguish populations. Since conserving
endangered species is inherently a "genetic" endeavor, to the extent that we recognize species as
discrete reservoirs of historically unique genetic material, the molecular approaches are very
useful.

BIOGEOGRAPHY

We have referred to pattern and process throughout different sections of this course. These
concepts are central to the study of biogeography which, in turn, incorporates many of the topics
in evolutionary biology. Biogeography often leads us to infer process from pattern.
Biogeography is the study of the distributions of organisms in space and time. It can be
studied with a focus on ecological factors that shape the distribution of organisms, or with a
focus on the historical factors that have shaped the current distributions. Certain regions of the
world have "Mediterranean climates" where ocean current and wind patterns hit the west coast of
N and S continents (Medit. region, California coast, Chile coast, SW Africa coast). Similar
climate has lead to convergent , but unrelated (by definition) types of plants. To make sense of
these types of ecological patterns we require a phylogenetic (historical) perspective: we need
tofocus on monophyletic groups.
The importance of a geographic scale was certainly appreciated by Darwin: the Galapagos
finches were morphologically distinct and geographically distinct and there must be a
connection. Moreover, the general view that speciation is a central phenomenon in evolution, and
that most speciation is allopatric speciation assumes that geography plays a central role: some
geographic feature divides a species range in two or more parts and over time speciation is
achieved (details in later lectures).
These sorts of observations were made by early biogeographers who recognized certain types of
distributions of organisms. Some species are restricted to a certain region and are referred to
as endemic species. Endemism needs to be defined with relation to the taxonomic group: all life
forms we know are endemic to the planet earth; the genus Geospiza (Darwin's finches) are
restricted to the Galapagos islands; Geospiza fortis is endemic to specific islands; the spotted owl
is endemic to the old-growth forests of the pacific northwest. Cosmopolitan species have a
world wide distribution. They may be restricted to specific habitats, but occur on most
continents.
In addition to endemism, another important pattern that needed to be explained were examples
of disjunct distributions where clearly related species (or even the same species) are found in
different areas. Marsupialsare found in Australia and South America. Ratite birds (Ostrich,
Emu&Cassowary, Rhea) are found in Africa, Australia and South America, respectively.
Alfred Russell Wallace noticed that different regions of the world had congruent patterns of
endemic species and he drew up six biogeographic realms (see fig. 18.2, pg. 510; nearctic,
neotropical, holarctic, ethiopian, oriental and australian). Wallace worked primarily in Malaysian
region and had noticed a clear break between Australian fauna and the fauna on the islands to the
northwest. This break has come to be known as Wallace's line (also a line between the
Australian and the Asian biogeographic zones). These patterns described long before continental
drift was an issue.
Different biogeographic areas can be quantified for levels of similarity in their biota
(biota=general term for flora+fauna, includes microbes). N
1
= number of species (or other
taxonomic unit) in one region, N
2
= number in another region (N
1
< N
2
) and C = number of same
species. Index of Similarity = C/N
1
. For Australia: New Guinea, I.S. = 0.93 (93%), while
Australia: Philippines, I.S. = 0.50 (50%). See table 18.1, pg 511. This provides a simple
quantification of Wallace's Line.
How do we account for these patterns? Early biogeographers tended to invoke dispersal (prior to
knowledge about continental drift). Potential problems: ad hoc, could pull dispersal out of a hat
whenever you needed to explain a peculiar distribution. Leads to many wild scenarios of "gravid
females" (pregnant, or inseminated females carrying eggs) making there way to distant
regions. Muddyfooted duck carrying propagules in its feet;land bridges invoked connecting
disjunct regions. Criticized by many as unscientific: cannot falsify the dispersal hypothesis
because it is something we'll never know for sure, thus is of no explanatory power.
Nevertheless, all these types of events probably have occurred at some point. The Bering land
bridge is well documented as an avenue of dispersal; the Opossum (a marsupial) in North
America clearly dispersed here from South America via the Isthmus of Panama (see below);
oceanic islands have life on them and it must have gotten there by dispersal. Several modes of
dispersal can be described: Corridors between two regions on the same land mass, Filter
bridges as selective connections between two areas, Sweepstakes as rare chance events (e.g.
muddyfooted duck).
Dispersal hypotheses often associated with arguments about centers of origin: those regions
with the greatest species (or higher rank) diversity. Greater diversity should be due to presence in
that region longer (more time for speciation), hence should be the region where the group
originated and from which dispersal events took place. Assumes that extant diversity
has not moved from origin of diversity. Possible, but not guaranteed for all taxa.
Alternative to Centers of Origin and subsequent Dispersal as a way to explain the current
distribution of species is vicariance where some barrier to genetic exchange causes the
separation of the related taxa. With the acceptance of continental drift, vicariance
biogeography became a discipline in which one could test hypotheses (see below). See models
in fig. 18.6, 18.8 and 18.9, pgs. 518-521.
As with most dichotomies in science: often need to invoke Both vicariance and dispersal to
account for distributions (not always in the same instance). Example: Galapagos finches had to
have dispersed to the archipelago from the mainland and in so doing imposed a vicariance
event on themselves. South American land bridge when sea levels dropped in the Pliocene the
isthmus of Panama rose and served as an avenue of dispersal for terrestrial mammals (the "Great
American Interchange" where unique N.American mammals dispersed to S. America and unique
S. Amer. mammals moved north, 3 mil. years ago; see fig. 18.14, tables, 18.2, 18.3, pgs. 528-
529), but served as a vicariance event for marine life that was distributed in the region. Lead to
the formation of Geminate species (species pairs on either side of the isthmus who are each
other's closest relative and were probably one species before the sea level dropped).
Pleistocene refugia nicely illustrate how vicariance and dispersal may need to be invoked to
explain current distributions. Glacial ice sheet forced species to new distributions (vicariance
event), after glacial retreat, the separated forms dispersed to previous regions (or wider
distribution). Relative roles of dispersal and vicariance in determining species distributions can
vary widely with a given species dispersal abilities (see fig. 18.3, 18.4 pg. 514-515). Essential to
realize that dispersal has two components: the ability to move and the ability to become
established. These two properties may not be "optimized" in the same organism.
Continental Drift as source of vicariance events. Evidence for continental drift provided by
disjunct fossil specimens: Mesosaurus in South America and Africa. Illustrates the space and
time component of biogeography since the strata reflect the same time (old) but are widely
separated in space. Continents must have moved. (Fig. 18.5, pg. 517).
Major stages of the split-up of continents: Pangaea formed in Permian (> 250 MyBP) and began
to break up in the Triassic (200 MyBP). Laurasia and Gondwana separated at
the Tethys seaway (135 MyBP). Tropical corals, sea grasses and mangroves are related in
Americas and old world tropics reflecting earlier Tethyan distribution. Gondwana began to break
up about 80 MyBP and the major continents were separated by late Cretaceous (65 MyBP). India
smashed into Asia crating the Himalayas. As the continents separated vicariance events
abounded and the fauna of various continents became increasingly Provincialized. The South
American mammals had many unique forms with respect to the North American Fauna.
Marsupials in Australian zone are distinct form of mammal.
Testing biogeographic hypotheses with cladistic analysis. Brundin's midges (fig. 18.7, 18.8, pg.
519-520) a classic in vicariance biogeography. Sibley and Ahlquist's Ratites and the Gondwana
breakup. Testing hypotheses about the sequence of vicariance events with cladograms from
several species. Validity of biogeographic hypothesis can be supported by congruence of
independent cladograms from unrelated species (see Cracraft, 1983, American Scientist vol. 71:
pg273). By considering the relationships of organisms and their geographic distributions, the
most parsimonious combination of the species cladograms can lead to an hypothesis of
vicariance events, a so-called area cladogram which presents the sequence of splitting events.
Using cladistic methods, one can test biogeographic hypotheses by asking whether area
cladograms for other, unrelated taxa are congruent. If different taxa all have similar area
cladograms (i.e., are "congruent"), then the sequence of vicariance events is supported. If one
taxon is represented in a region where none of the other taxa are found, then one might be forced
to invoke dispersal to account for the disjunct distribution. The strength of this approach is that
hypotheses are testable and one need not resort to ad hoc explanations that should be taken on
faith. Biogeography can be practiced in a scientific manner despite its historical nature.

EVOLUTION AND DEVELOPMENT I: SIZE AND SHAPE

First, some general background to the study of development and evolution. Evolution of
organisms involves a change in the developmental program, a change in a series of
developmental processes. We often refer to evolution as "descent with modification" and the
modification we often notice first is the overall appearance of the organism. This appearance is a
result of the development of the organism, thus evolution is intricately involved with
development.
Embryology played a major role in evolutionary theory in the 19th century, but was largely
ignored in the 20th. Development never really became part of the modern synthesis. Some argue
that this is due to the lack of communication between geneticists and developmental biologists.
The geneticists were concerned with the rules of transmission of genetic material between
generations and the developmentalists were concerned with cellular changes that led to the
transformation of an egg into an adult organism. Mutations in adult phenotype were readily
available for the study of genetics, but there were precious few "developmental mutants" that
bridged the gap between development and genetics (such mutants were discovered in growing
numbers during the formulation of the "Modern Synthesis", and many more discovered later).
The general approach is the same as we have taken with the evolution of other traits:
development has a genetic basis, if there is genetic variation for the developmental program then
development can evolve. We will first take a descriptive approach to evolution and development
and next lecture look at some of the more genetic and cellular mechanisms of development.
Early embryologists noticed similarities between ontogeny (the development of an organism)
and phylogeny (ancestor descendant relationships in a group). The common phrase "ontogeny
recapitulates phylogeny"was put forward by Haeckel as his biogenetic law (see fig. 21.3, pg.
588). Haeckel held that descendants, during their ontogeny, passed through stages that resembled
the adults of their ancestors. Before this, Cuvier(1812) held that there were four major classes of
organisms: vertebrates, mollusks, articulates and radiates. Cuvier noticed that there was nothing
in the ontogeny of a vertebrate that resembled the adult stages of, say, a mollusk. This is because
evolution is a bush or a tree not a "ladder" of the great chain of beings. This "branch-like"
pattern to phylogeny was apparent to Haeckel, but he still claimed there was "recapitulation".
von Baer made observations about ontogeny and phylogeny that seem obvious to us today, but
they are important in development and evolution as they run counter to recapitulation: 1)
more general characters appear early in development, 2) less general forms develop from the
more general forms, 3) embryos do not pass through other forms they diverge from
them, 4) embryos of higher forms only resemble embryos of other forms (human, calf, chick
and fish look similar at embryo stage but diverge quickly). See section 17.8.2, and fig. 17.11,
pgs. 478-479.
Putting these two views together, we see that there can be a sort of recapitulation within a
lineage (i.e., within an evolutionary sequence of ontogenies) but there are many examples that
refute the notion that phylogeny is reviewed during ontogeny.
First efforts to place development and evolution in a quantitative, descriptive context were
provided by d'Arcy Thompson in On Growth and Form. Using simple rules of geometric
transformation he showed that one could obtain the varied forms of organisms by "warping" or
"bending" the relative positions of their body parts (see fig. 21.10, pg. 599). These types of
diagrams are helpful in identifying what changes of form have taken place, but they do not
identify how developmental mechanisms have evolved (the same criticism might be leveled
towards Raup's computer snails (see figures 13.7 and 13.8, pgs. 356-357), but mechanism was
not the intention of these approaches).
One thing Thompson and Raup's diagrams did contribute was to focus attention on the notion
of size and shape. These two very simple words are deceptively complex in the context of the
evolution of development. A general paleontological pattern is Cope's rule which states that the
body sizes of species in a lineage of organisms tend to get bigger through time. Horse evolution
is a classic example. But what happens when you get bigger? In most cases body parts do not
grow at the same rate, thus we have allometry.
Allometric growth is the differential rates of growth of two measurable traits of an organism
(often it is described as size-correlated changes in shape). It is quantified as y = bxa where x is
the measure of one trait, b is a constant, a is the allometric coefficient and y is the other trait. In
this form it describes a logarithmic relationship. It can be made into a linear relationship by
taking the logs of the values measured for each trait (or by plotting on log x log graph paper):
log y = log b + a log x. This is the equation for a strait line with a being the slope of the line.
When a<1 we have negative allometry which means that as x gets bigger, y gets bigger at
a smaller rate. When a >1 we havepositive allometry which means that as x gets bigger, y gets
bigger at a faster rate. When a=1 we have isometry (or isometric growth) which means that there
is no change in shape (i.e., the relative sizes of body parts) during growth. See fig. 21.9, pg. 597.
We can describe different kinds of allometry: 1) interspecific allometry where traits of
individuals of the same age (usually adults) are compared between different
species, 2) intraspecific allometry where a) traits of individuals of all ages are compared within
a species (also called ontogenetic allometry), or b) traits of individuals of the same age are
compared within a species (also called static allometry).
Some examples: interspecific=the Irish elk example (more below), intraspecific
(static)=measurements of body height and arm length in class, intraspecific
(ontogenetic)=measurements of body height and arm length with my daughter's day-care
measurements included. See figure demonstrating ontogenetic and interspecific allometry of
brain and body weight in the same graph.
Intraspecific allometry just describes growth, and alone is not an evolutionary comparison. It is
of interest that the allometric coefficient of Bio 48 males and females is ~ 1.0, but if the toddler
data are included the allometric coefficient goes up to ~ 1.3. This means that as adults we have
about the same proportions (a=1) but as we grow from infant to adult, our arms get
proportionally longer (a=1.3).
Allometry is useful in describing the evolution of size and shape. Different species attain
different morphologies by virtue of different timing of various developmental processes. This
change in timing is calledheterochrony. Figures 21.5 - 21.8 and table 21.1, pgs. 590-594 review
some of the typical examples of heterochrony. Using the figure below, we can group these into
two general classes: in figs B and C the ancestor (dotted) and descendant (solid, but hard to see
in C) have the same slope but the descendant stops growing (=adult) at a different time; in figure
D and E, the descendant grows for the same amount of time (in these cases same amount of x but
different amount of y) but at a different slope. Both are heterochronic changes because some
aspect of timing (relative or absolute) has changed in evolution.
Notice that each axis of these graphs include both a measurement component and a time
component simply because growth by definition is both a temporal and a dimensional
phenomenon. Note that only one of these examples of different growth plans (graph B)
demonstrates "ontogeny recapitulates phylogeny": hypermorphosis. Therefore, shape
changes can be observed as 1) changes in the slope of an allometric relationship, or 2) changes
in the y intercept of an allometric relationship. Recalling high school algebra, a change in the
slope will change the intercept, but the intercept can be changed without changing the slope
(keep the line parallel and move it up or down). All of these changes result in change in shape.
Even with the same slope but different intercepts the relative sizes of x and y will be different so
there will be a change in shape. The only case where there is a change in size with no change in
shape is when the allometric slope = 1.0 and growth continues (or retards) relative to the
ancestor.
Classic examples of allometry are neoteny in human evolution: as adults we look like the
juvenile stages of chimps; and neoteny in salamanders: the adult of descendant retains gills (a
juvenile morphology in the ancestor). Peramorphosis in the evolution of deer: the "Irish
elk" (actually a deer) has phenomenally large antlers and are "disproportionately" large because
there is an allometric relationship between body size and antler size. In fact the Irish elk falls
right on the line of allometry for other species in the family (interspecific allometry). Thus, the
antlers are larger than usual, but they follow precisely the developmental program that seems to
be a part of its phylogenetic group. Previous adaptive (and maladaptive) stories had been told
about these huge antlers and how they probably drove the elk to extinction, thus a challenge for
"adaptive" evolution, but the allometry shows that they are not really "abnormal" (probably went
extinct due to climatic changes and hunting). See discussion on pg. 356-358 of adaptive, vs. non-
adaptive explanations of morphology.
Allometry is also important in the context of the criticisms to the "adaptationist program". If you
looked at a Titanothere with its bizarre horns pointing out of its snout, you might say "what are
those things for" as if they evolved for some function. They may not be "for" anything but
simply the result of a positive allometric relationship between body size and horn size during
evolution. Now the question becomes: what causes Cope's rule? Since allometry is so
common, changes in size will produce changes in shape.

EVOLUTION AND DEVELOPMENT II: GENES AND MORPHOLOGY

Documenting allometry and patterns of size and shape changes in evolution are helpful as
descriptive approaches to the evolution of development. But these phenomena are themselves
the result of developmental mechanisms at the molecular and cellular level. We can often say
without reservation that there has been a change in development during evolution, but how that
change in development was achieved is yet another question. We improve the description
somewhat by saying that changes in development result from changes in the: 1) spatial
organization of cells, 2) timing of gene action and tissue differentiation and 3) geometry of
tissues and organs. But how are these changes mediated?
Consider the comparison between humans and chimps: the adult morphology is obviously
distinct, but at the genetic level we are extremely close to chimps: >99% similar at the genetic
level. This is less genetic divergence that seen between sibling species (can't tell them apart) of
Drosophila and some mammals These observations indicate that morphological evolution has
proceeded faster than molecular evolution suggesting thatregulatory evolution has proceeded
faster than DNA sequence evolution. Where are the important mutations (short arrows)? in the
coding sequences of genes or in the regulatory sequences upstream from them? May depend on
how the product of a gene interacts with other genes (longer arrows).

Thus perhaps the key to understanding the evolution of development is the study the evolution of
the genetic regulatory mechanisms that control development. Now the question becomes: what
do we know about genetic regulation of development?
A fair amount is known in Drosophila. The exciting point here is that in recent years there have
been increasing numbers of papers describing the existence of gradients across the egg or early
embryo in the concentration ofspecific proteins encoded by a handful of loci. These proteins can
be thought of as morphogens ("form creators"), molecules that, for years, were postulated to
exist by embryologists. With a gradient across the embryo of such a morphogen, there is the
possibility the other proteins that might interact with such a morphogen can obtain position
information from the gradient such that high concentration means "anterior" (or "limb end" in
vertebrate limb bud) and low concentration means "posterior" (or "limb base").
The significant point in all this is that Drosophila geneticists have been able to identify
specific developmental mutations (mutations in the genes that code for morphogens, or genes
that code for molecules that interact with morphogens) that disrupt specific events in
development. One such example is the bicoid gene: when this gene is mutated, its normal
gradient is disrupted and the embryo has two tails (bi-caudal). The point is that there are specific
genes that determine the major body axes and one can envision that evolution of major new
developmental programs might proceed by naturally occurring mutations in these genes that
would move/alter the gradient, or, equally as significant move/alter the cellular localization of
the receptor of a morphogen.
On a more theoretical level, morphogens have been hypothesized to operate in a threshold-like
manner in more localized examples of pattern formation such as the generation of additional
bristles in Drosophila or specific patterns of striping in mammals (see figs. below). Specific
molecules causing "prepattern" such as one sees in zebras have yet to be identified, in contrast to
the major advances made in Drosophila, but mating zebras is a major undertaking.
There is solid support for such ideas in Drosophila development. The RNA encoded by
the bicoid gene is localized in the anterior portion of the embryo. The protein translated from
this localized RNA is distributed as agradient from anterior to posterior across the embryo.
The bicoid protein affects the distribution of the RNA of another gene, hunchback. This RNA
(hunchback) is not distributed as a gradient but in a discrete way: present in the anterior, absent
in the posterior. Thus there appears to be positional information in the concentration
of bicoid which is read by hunchback as a threshold. One could imagine that a mutation that
affected the localization of one morphogen could alter the localization of important thresholds of
different morphogens, which would in turn lead to the development of new morphologies.
The genes controlling the early events in the development of Drosophila can be classified into
three broad categories: Gap genes are a set of genes that act to define broad regions of the early
embryo; these can regulate the expression and action of Pair rule genes which further define the
broad regions into more numerous segments; the pair rule genes can affect the expression and
action of Segment polarity genes which will determine the fate of certain structure within each
segment. As with the gradients of morphogens described above, one can envision mutations that
alter the interactions between these broad classes of genes controlling the developmental fate of
parts of the organism which, if established in the population, could lead to the evolution of new
morphological "plans" (.g., a new Bauplan).
There is good evidence for such a supposition in another very important set of genes:
the homeotic genes. Certain mutations in these genes result in homeotic mutations where one
body part is transformed into the structure of another body part. The best examples are
the Antennapedia complex and the Bithorax complex which are large regions of the
chromosome containing several genes each. The positions of the genes on the chromosome have
a remarkable correlation with the segment of the body in which they are active! (see figures
below). The genes contain a region of DNA that codes for a highly conserved stretch of amino
acids, known as the homeobox that generally are involved in the determination of body
segments (but bicoid has a homeobox and it is more involved with anterior-posterior
determination). While mutations that move a leg to the position of an antenna (in the
Antennapedia complex) or transforms the balancing organs (halteres) into a pair of wings (in the
Bithorax complex) is of dubious fitness value to the organism, it does show that modifications of
the general body plan be achieved by mutations in one or a few genes, i.e., there is genetic
evidence that Hopeful (hopeless?) Monsters could be produced.
These phenomena are compelling in light of the belief that arthropods (insects, crustaceans, etc.)
evolved from annelids (segmented worms; see figure below). One can envision that sequential
modification of body segments, through mutations such as those described above, might allow
for the evolution of insects from a worm-like ancestor. Suggestive of this is the observation that
when the Antennapedia complex and the Bithorax complex are mutated the larval stage of the
fruit fly is transformed into a larva with many thoracic segments rather than the wild-type pattern
of differentiation into maxillary, labial and abdominal segments (see fig.below). This "throw
back" to the ancestral form (i.e., the middle segments of worms are relatively undifferentiated) is
called an atavism.
In thinking about all possible morphologies one might be able to get with bizarre mutants in
flies, and looking out at the incredible diversity of form in the natural world we might best think
of this problem in terms of the question: why this and not that? Are there forbidden
morphologies that development cannot produce?. There is some nice evidence that the different
forms seen between species may be the result of the "playing out" of discretely different
developmental programs. When the developing limb bud of one salamander is treated with an
inhibitor of mitosis, the number and pattern of digits developing resembles that of another
species (section reading). This suggests that there are developmental constraints, i.e., that
development is constrained to proceed in a certain way. If different developmental programs are
carried by different lineages of organisms as they diverge from one another, these developmental
constraints become phylogenetic constraints: there is no chance that horses will sprout wings
because the lineage of horses (and ungulates in general) are constrained to develop and use their
forelimbs in very different ways than bats, lets say.
A conceptual model for this notion of constrains is to think of there being canalization of
developmental programs. Waddington's model of development as a ball rolling down a landscape
suggests that the program is canalized to follow a particular
trough. Mutations and/or environmental fluctuations (next lecture) might knock the ball around
in the trough, and if these perturbations were strong enough might throw the developmental
program over into a new canalized ontogeny. In this model the location of the troughs suggests
that events that perturb development early on are more likely to result in major changes in the
developmental plan. Perhaps developmental programs become more "canalized" as they proceed
through development. This is of particular significance in light of the network of genes described
above that establish body plan during earlyembryogenesis.

PHENOTYPIC PLASTICITY AND NORMS OF REACTION

Phenotypic plasticity is the ability of individuals to alter its physiology, morphology and/or
behavior in response to a change in the environmental conditions. This is clearly demonstrated
by the appearance of plants grown at different densities: crowded plants look spindly and lanky,
uncrowded plants look healthy and robust. In the context of evolution, phenotypic plasticity
demonstrates the two meanings of adaptation: the plastic response is itself an example of
a physiological adaptation and it is widely held that the ability to be plastic is adaptive in the
sense of increasing fitness.
In thinking about phenotypic plasticity as a evolutionary adaptation it is important
to separate the trait in question from the plasticity for that trait. For example: growing taller
in response to plant crowding is adaptive in the sense that it increases an individual's competitive
ability for sunlight (lower fitness when shaded by other plants). The "normal" height for a plant
(lets assume there is such a thing) may have evolved in response to pressures to allocate
resources to growth versus reproduction in a particular way. Thus there is a genetic basis
for plasticity of plant height, and a genetic basis for plant height itself. The point is that different
genesprobably control these processes so the trait and its plasticity can (as opposed to must)
evolve independently.
Now consider the environment: certain physical properties of the environment can be described
by the mean (average) value or the range of values (highest - lowest). Which aspect of an
organism (the trait itself or the plasticity for that trait) will evolve in response to which measure?
It may be that the plasticity for a trait will evolve in response to the range of values the
environment throws at an organism (e.g., coldest - hottest, driest-wettest days), whereas the trait
itself (e.g., thickness of fur) will evolve in response to the mean. This is not a rule! but would be
an interesting thing to test and/or think about.
The idea of plasticity is interwoven with the notion of canalization. In light of the ball rolling
down the trough of a developmental pathway (previous lecture), one can consider the width of
the trough as an indication of the amount of plasticity "tolerated" in the organism in question.
A highly canalized organism (or developmental program) would have low plasticity.
Another variant form of the plasticity issue is that some organisms may exhibit threshold
effects where there is not a clear gradual transition between forms, but a stepwise change of
phenotype in response to a gradual environmental change. See fig. 9.11, pg. 242, but note that
these graphs do not have an environmental axis, so a distinct from a norm of reaction. One
example of this are plants that have distinctly different growth forms in different environments.
Question: is there an "environment" that is half way in between air and water?, and if so would
these plants exhibit a graded response to such an environmental gradient?
A concept that places phenotypic plasticity in the context of a genotype-specific response is
the norm of reaction. A norm of reaction is an array of phenotypes that will be developed by a
genotype over an array of environments. The quantification of a norm of reaction is conceptually
quite simple: one obtains a number of different genotypes (clonal pants are great for this) and
grows each one in a variety of different environments (e.g., different nutrient, light, water
conditions). After a period of growth one measures the desired trait(s) from each individual and
plots the data out as shown in figure below; this case for Drosophila bristles. Each line represents
the data for a different genotype. If all lines are perfectly horizontal and on top of one another
there is no effect of environment (E) or genotype (G) in case 1 below (each genotype is x, y or
z). If all lines are not horizontal but on top of each other there is an environmental effect, but no
genotype effect (case 2). If all lines are horizontal but at different positions there is no effect of
environment but there is an effect of genotype (case 3 below). If lines not horizontal but are
parallel there is an effect of environment and genotype, but there is no genotype x environment
interaction (figure and case 4 below). If the lines are anything other than horizontal, there is an
effect of environment. If the lines are neither horizontal nor parallel there is an effect of I)
environment (nonhorizontality), ii) genotype (lines not on top of each other) and iii) genotype x
environment interaction (not parallel; case 5 below).


The interesting case comes when the norms of reaction lines cross. Then there is a range of
environments where genotype 1 is "bigger" than genotype 2, where both genotypes are about the
same and where genotype 2 is "bigger" than the genotype 1 (see figure below). Thus determining
what is the "best" genotype, or the "fittest" genotype depends on the environment.

EARTH HISTORY (NOTE: this material covered in lecture on Origin of Life & Fossil Record)


Much of evolutionary biology involves the history of organic diversity. Organic diversity has
been shaped and affected by the origin and history of planet earth. To appreciate this history we
need to acquire some knowledge of the geological processes that have shaped the earth. One
general theme to consider in this and the next lecture is: if we were to start the history of earth
over again from the "primeval soup" would the results be the same? Almost certainly not (see
Gould, 1989. Wonderful Life for a detailed discussion). History is unique and events
are contingent on what has occurred previously. Much of the contingency of organic evolution
is dependent on the unique series of events that shaped the earth, this is why we need to
understand some basic geology.
How was the planet formed? What is its relationship to other matter in the universe? A popular
hypothesis for the formation of the earth is the nebular hypothesis. This idea dates back to the
philosopher Immanuel Kant (1755) and Laplace (1796) and has been modified as empirical
evidence and theory mount. Recent incarnations (chemical -condensation-sequence model) start
with the solar system forming from a rotating, diffuse cloud of dust and gasses (a nebula). As the
nebula cooled the matter condensed into "planetesimals", near the sun where temperatures were
highest elements with the highest melting points (metals and heavy minerals) condensed first.
Lower melting temperature elements and compounds (water, methane, ammonia) condensed
more readily in the cooler areas further from the sun. This helps to explain the density gradient in
the solar system, the closest planets to the sun are terrestrial while those further away are
gaseous.
How did the earth form in the condensing nebula? The earth may have formed through the
accretion of many planetesimals and as the mass increased through gravitational attraction and
compression (overhead). The earth was probably initially a homogeneous ball that heated from
three sources: 1) energy of planetesimal impacts, 2) gravitational compression lowered potential
energy releasing heat, and 3) heat from radioactive disintegration (20 cals is released for 1
cm3 of granite over 500 million years). As the earth heated it began to differentiate into various
zones of matter with different properties (overhead). Differentiation was possible because
molten material could rise or sink depending on density, be moved by convective currents, and
localize due to chemical zonation (overhead). As the earth cooled outgassing of the mantle
released compounds (water vapor, carbon dioxide, hydrogen, nitrogen) into a primitive
atmosphere.
Early geologists tried to determine how old the earth was from observations about the features of
the earth. Age = Thickness of sedimentary rock/rate of sedimentation. Old (<1.5 billion years)
but not old enough. Age = salinity of sea/rate of salt deposition in seas. Again old, but not old
enough. Lord Kelvin (of absolute zero fame) calculated the age of earth from its temperature,
assuming it was molten at its formation. Gave 100 million years (and gave Darwin a bit of a
problem: was this enough time?? Radioisotopes cleared things up (see below)
We can divide the processes that alter the earth's surface into two categories:
1) igneous processes (volcanism and mountain building) construct features by increasing the
average elevation of the land, 2) Sedimentary and erosive processes (deposition and
weathering) act as forces wearing down features created by volcanoes and creating new
horizontal features (e.g. river delta). The theory of Plate tectonics provides a synthetic model for
understanding how the dynamics of the earth work. The plates move around, collide, move over
or under one another. Divergent boundaries are where plates move
apart, convergent boundaries are where plates move toward one another, transform boundaries
(e.g. San Andreas fault) are where plates move by each other. The continental plates
(lithosphere) float on molten inner layer (asthenosphere). Where plates meet there can be
uplifting or subduction. Uplifting results in mountain building through igneous activity and at
the boundaries between plates and actual scraping off of material from the subducted
plate. Subduction results in plates being forced downward and is seen is formations such as
ocean trenches.
The rock material of continental plates can be viewed as going through a rock cycle that can be
related to plate tectonics. Magma (molten rock) e.g., released from volcanoes, crystallizes and
forms igneous rocks ("fire formed rocks"). Through weathering and transport sediment is
formed which by lithification become sedimentary rock. Through exposure to high temperatures
and pressure, sedimentary rock (or any rock) can be changed into metamorphic rocks. If this
rock is exposed to extreme temperatures it can become molten again and form magma, and if
released through volcanic activity be reintroduced as igneous rock.
In what kind of rock would we expect to find fossils? Sedimentary rocks. Their structure can tell
us a lot about earth history. Laid down in strata of sedimentary layers. Bedding
planes generally mark the boundary between the end of one sediment and the beginning of
another.
Several logical rules can be used to determine the sequence of events: Relative dating. generally
one follows several principles: superposition the older rock is below and the younger rock is
above; original horizontality: the strata are laid down originally in a horizontal position (gravity
is what lays them down). Thus nonhorizontality must have occurred after the deposition. The
cross cutting relationship states that the cut formation is older that the formation doing the
cutting.
Another prominent feature is an unconformity which occurs when the rate of deposition has
been interrupted, the sediments eroded and deposition renewed. A clear break in the sequence of
events is apparent. One type of unconformity is an angular unconformity where strata with
originally horizontal bedding planes now have bedding planes that intersect. Significant because
it reflects a major episode of geologic change.
All well and good for a given formation, but one would like to be able to make general
statements about larger regions. This can be done by correlation of strata from different
formations separated by some distance. Stratum "X" may lie near the top of one formation and
many miles away, X may be found near the bottom of a new formation, at the top of which is a
different layer "Y". Several miles further on, "Y" may lie at the bottom of a third formation, and
in this way one can link or correlate the different strata.
This may work for a large region but one would like to do this for the entire earth. It turns out
that there are diagnostic fossils found in different formations around the world. These Index
fossils help correlate different formations on each of the major land masses. This was recognized
by William Smith (see lecture 2). The phenomenon is more pronounced than an occasional fossil
here and there: entire biotas go through successive changes in sequential strata, illustrating
the principle of faunal (biotic) succession. We thus have the "age of trilobites" seen early in the
fossil record. Later the age of fishes, age of reptiles, age of mammals are clear in formations
around the world indicating the comparable ages of formations separated on different continents.
These fossil beds lead to the formation of the Geologic time scale, the names of each period
deriving from the locality where the characteristic formation was found. The major divisions
(eons, eras) are defined by the presence or absence of fossils: proterozoic, phanerozoic (visible
life or animals). Geological dating is often problematic because geologists use fossils to date
rocks and biologists use rocks to date fossils. A measureindependent of stratigraphy and fossil
remains is necessary. With the discovery of radioactive decay it became apparent that one could
use the ratio between the parent isotope and the daughter product (e.g., U238decays through
several steps to Pb206). By measuring the amount of isotope and daughter product and knowing
the half life of the isotope one can estimate the absolute age of a rock formation. Problems:
when the daughter material escapes and hence produces an inaccurate estimate. Additional tests
with different isotopes can corroborate one another.

ORIGIN OF LIFE AND THE FOSSIL RECORD

A brief review of salient points regarding the origin of life:
Cosmic calendar: Earth formed 4.6 billion years ago; there has been a long time for life to
evolve. It took about a billion years to get through the early stages of chemical evolution such
that there is some form of self-replicating system (e.g., a primitive living thing in its simplest
definition). Miller experiments lead to formation of amino acids under lab conditions
simulating a primitive earth atmosphere. Subsequent reactions could produce short polymers of
the amino acids. When polymers are heated to 130C to 180C and then cooled in water to 25C
- 0C proteinoid microspheres form. These provide evidence that simple cells could have
formed from some of the earliest compounds.
Progress has also been made on the synthesis of nucleic acids. One significant bit of evidence,
much further down the line, was the discovery of catalytic RNAs that performed enzyme like
functions. This, and other evidence, suggested that RNA may be ancestral and DNA is a derived
molecule for the storage of genetic material.
By 3.2 billion years ago, first procaryotes (Bacteria, blue green algae). By 2.5 - 2.0 billion years
ago, communities of procaryotes emerge. e.g. Stromatolites as colonies of Blue green algae,
formed biosedimentary domes of calcium carbonate = some of the earliest fossils. Photosynthetic
bacteria have significant effect on the earth's atmosphere and the subsequent evolution of life.
Blue green algae are photosynthetic and produceoxygen as a waste product. This was initially a
poisonous molecule (as environment was an anoxic one) Lead to the production of an oxidizing
atmosphere.
Large amounts of Oxygen oxidize the vast quantities of dissolved iron in the oceans: i.e., the
oceans "rust." This counteracts the poisonous atmosphere problem, but only until the reservoir of
iron is depleted and the iron settles out as the banded ironstone formation = layers of iron
which form iron ore deposits. Ultimately, with the absence of iron to oxidize, the oxygen builds
in the atmosphere and produces an ozone layer. This is a singular event which eukaryotes will
ultimately take advantage of in the form of oxidative respiration. Subsequent cellular (at this
time = organismal) evolution is contingent on this singular event. If we started earth over again,
would this event re-occur? at the same time?, if not would we have evolved???
1.5 Billion years ago, a diverse flora of Eukaryotes present as asexual species. 1.4
By eukaryotic algae present. First metazoans seen in the Ediacara fauna for Australia (680
MyrBP).
Before considering the diversity of fossils we need to think about how representative the fossils
are of past life which is largely a function of what gets preserved and where it might get
preserved.
What gets preserved? Hard parts, and other parts that can be mineralized. Sequence of events
from death to scavenging to decay to covering with soil. Example from heard of elephants:
"wet" stage = two weeks (too much tissue for vultures so many invertebrates helped out). By the
end of the third week, Dermestid beetles had removed all the skin and sinew from the bones.
Within five weeks the temperature fluctuations caused the bones to crack and flake. Within one
year the skeletons were completely disarticulated. Within two years many bones were covered
with soil. Current day events can shed light on the fossilization process.
Fossilization: percolation of mineral grains (e.g. calcium carbonate) into interstitial spaces of
hard part tissue. In bone the mineral is calcium phosphate which can incorporate fluorine, present
in minute amounts in water, into the Calcium Phosphate to produce a crystal more resistant to
erosion.
Death assemblage: become fossils at a site away from their actual habitat due to death and
transport to an area. Life assemblage: organisms preserved in their natural habitat. Obvious
example: If large mammal bones were found scattered among fossil fish, one presumably
would not invoke the existence of primitive mammals that walked on lake or ocean floors!
Environments: fossils are generally restricted to areas of deposition. Upland areas less likely to
preserve fossils: more erosion. In deserts material is covered by sand and has a good chance of
being fossilized. Inshallow seas sediment is being deposited and can cover skeletons. Some of
the best fossil assemblages are from shallow sea deposits, lake beds, outwash plains from
periodic river floodings, etc.
Ediacara fauna (640 MyBP) Many forms that bear some resemblance to modern phyla. Appears
as if it were a major "evolutionary experiment" that did not work as it appears that none of their
representatives made it into the Cambrian.
Burgess shale (530 MyBP, British Columbian rockies) Discovered in 1909 by Charles Doolittle
Walcott: remarkable diversity of many different forms. Some of these are represented today
many others are not (about 15-20 distinct, and now extinct, phyla). e.g. Hallucigenia, Opabinia,
Yohoia, Pikaia (first chordate), etc. Nicely illustrate the nature of Contingency (see S. J.
Gould, Wonderful Life, 1989, Norton). The "iconography of the cone" led Walcott to erroneous
pigeonholing of the Burgess shale organisms into "known" groups. The more appropriate image
is "decimation" where only some organisms get through alive and those that do may be simply
lucky. Harry Whittington in the 1960s and 1970s with Simon Conway Morris in the mid to late
1970s reanalyzed Walcott's collections. Concluded that there were many unique morphologies so
new that they deserve the status of new phyla!. Many of Walcott's classifications were wrong.
What would have happened if Pikaia had not made it through the "decimation"? (would you be
here reading this? Another example of contingency).
Other important points in interpreting the fossil record: Dating fossils requires radiometric dating
of associated igneous rock. (sedimentary rock is of highly mixed origin). Moreover, fossils and
the bed in which they lay have been reworked and redeposited. Careful stratigraphy and analyses
of surrounding strata must be done to provide meaningful data about
the relative and absolute ages of fossils. Gaps in the record. The nature of the fossilization
process almost assures that there will be gaps in the fossil record. We have to live with it.
What do we know about fossil organisms? Certain associated information allows informed
speculation about the biology of fossil organisms. Large dinosaurs that left tracks without tail
dragging marks suggest an active lifestyle? (other fossil remains do show clear evidence of tail
dragging and footprints). Other assemblages show fossil bones of adults associated with nest
sites and eggs: suggests parental care? Simple footprints may seem like a cute form of fossil
evidence. Actually a lot can be learned about the organisms: one can corroborate estimates of the
animal's size; one can measure distance between prints and obtain information about gait, travel
speeds, etc.; these interpretations further dictate a host of different physiological processes that
might be able to sustain such a manner of locomotion. These types of issues are the main point of
this lecture: from a small amount of fossil information, certain biological interpretations are
implied simply by the necessary biological attributes that go along with a given footprint size,
shape, etc.
Fossils can help define ancestral character states and thus help clarify relationships of extant
organisms. However, this cannot be done without the extant organism's character states (i.e.
fossils alone aren't much help. Is Archaeopteryx birdlike enough to be considered a bird
ancestor?

CLONING DINOSAURS

What is a Dinosaur? 1) occured from the mid-late Triassic to the end of the Cretaceous (220 mil.
years ago, mya to 65 mya) 2) they are "reptiles", (but as we know this is not a natural group), 3)
they were terrestrial (excludes marine plesiosaurs, ichthyosaurs, mososaurs, 4)
Upright pillared legs (an obvious structural "necessity" given their weight. Only the latter is a
good "defining" character, cladistically, since there are plenty of other organisms that fit
descriptions 1-3 that are not dinosaurs. Moreover, some mammals and birds have pillared legs.
There are two general groups of dinosaurs based on hip morphology The Saurischia (reptile-
hipped) and the Ornithischia (bird-hipped). In both groups the ilium and the ischium have
relatively similar forms, but in the Ornithiscia, the pubis has a narrow rod-shaped extension
running ventrally and posteriorly along the ventral side of the ischium. In the Saurischia, the
pubis extends ventrally and anteriorly and only articulates with the ischium (and ilium) to form
the hip "socket". Most of the Ornithischia also have a horn covered beak and bony rods and
vertebral spines.
Within each of these two major groups there are further distinct types. Within the Saurischia
there are two major groups the Therapods (beast-foot) and the Sauropods. Typical Therapods
are Tyrannosaurus rex,Deinonychus. These are carnivorous, have bird-like feet, bodies are
balanced at the hip with a long powerful tail. Within the Sauropods are the huge species such
as Apatosaurus (~Brontosaurus) and Brachiosaurus. These walked on all fours, had long whip-
like tails and were herbivorous.
Within the Ornithischia there are five major groups:
Ornithopods e.g. Hadrosaurs, duck-billed dinosaurs
Ceratopians e.g., horned and frilled dinos such as Triceratops
Pachycephalosaurs with large bone-filled heads
Stegosaurs (e.g., Stegosaurus) with large dorsal spines of disputed use in thermoregulation
Ankylosaurs heavily armored and abundant in late Cretaceous
The only living relatives of Dinosaurs are Birds. From the names of the two groups one might
expect that the birds descended from the Ornithischians. This is not the case. Birds are related to
Therapod dinosaurs. The living sister taxon to birds are Crocodylians; how do they fit in? You
probably think of Pterosaurs as dinosaurs, too, but they are not. Below is a simplified cladogram
of relationships.



Cloning Dinosaurs - Can it be done?
What do we need to do? What are the "parts" needed?
- DNA, in the form of an entire Genome
- Cell
- Technology for putting these together
With the right combination of DNA and cell, it could work
BUT: a genome and a cell are remarkably complex "parts"
However, if you wanted to do it, Crichton's (Poinar/Wilson) approach is a plausible one
Technology:
Dinosaur DNA from fossil bones and cells of dinosaurs in the bodies of blood sucking insects
trapped in amber
DNA extraction - remove tissue from amber with sterile tools, grind tissue in sterile
homogenizing buffer, dehydrate and then dissolve in buffer solution.
Vector Cloning: cut DNA into pieces, splice fragments into a cloning vector, introduce
vector+DNA into bacterial cells where many copies are made in cell culture
Remove Dino DNA from vector and reassemble DNA fragments by splicing (ligation)
Assemble complete chromosomes by filling gaps with frog DNA
PCR (Polymerase Chain Reaction): Amplify random fragments of DNA, then clone
Genome: If we do get DNA:
A. what species of DNA is it? = A molecular systematics problem
identify DNA by its affiliation to putative extant relatives
characters, shared derived character states, group membership
Could be different parts of different taxa: DNA extracted could be a mixed bag of different
dinosaur species and other vertebrate taxa different. Probably not enough taxonomic resolution
to determine the species identity of the DNA sequence. This is important: how do you tell
whether a chunk of DNA is Tyrannosaurus or Stegosaurus simply based on phylogeny of these
sequences if there are no living members of either linage to provide a basis for discrimination
Here's where bones are key: species (at least genus?) identify available AND the DNA for the
same sample.
B. What part and percent of the genome is it?
Coding DNA and Genome Size, C-value paradox, Numerology:
- Genome Size: 1 - 10 x 109 base pairs in a sperm or egg cell (twice that in "diploid" cell)
- Number of genes: 50,000
- Average gene length: 1,000 base pairs
- Genome is mostly "Junk DNA": 50,000 x 1,000 = 50,000,000
- Coding DNA = "2% of the total genome
- Largest fragment recovered: " 300 base pairs of only two kinds of genes
- Percent of genome recovered: 1 / 10,000,000th of the genome in base pairs
- Percent Coding DNA recovered: 1 / 166,667 Actually less since there are introns
Cell: Which species of cell?
How do the proteins and other molecules of one species interact with the DNA/genes of another
species (will Dino+frog DNA function properly in modified crocodile eggs??)
DNA as a generative program: does the DNA alone cary the info. to tell any old cell how to
make a dinosaur? Development involved many important tissue inductive events.
Tissue specific gene expression: Liver cells express liver genes, blood cells express blood genes
De-differentiation: easy in plants; rare in animals. Mitotic arrest: who says the cells will keep on
dividing? These are Big problems; it will be some time before we clone dinos.
Of all the problems, the Phylogenetic problem of knowing the species identity of any cell from
an insect's gut is as serious as the technical problem of getting the DNA in the first place! A
reconstructd dinosaur might well wind up as part Ceratopian, part Sauropod and part Therapod
(assuming mosquitos were not super host-specific).

PATTERNS OF DIVERSITY

To appreciate the temporal scale of the phenomena that we will discuss, we should review the
geologic time scale and the major eras (Paleozoic, Mesosoic, Cenozoic) and periods (Cam Or
Sil Dev Car Per Tri Jur Cre Ter Quat) and epochs (Pal Eo Oli Mio Plio Pleisto Holo). The point
here is that there has been immense amounts of time in earth history (recall our 15 second
moment of silence in class as one frame of reference). Each of these geologic time periods is
defined on sedimentary evidence, much of which is comprised of fossils characteristic of each
time period.
On ridiculously simple terms, there has been a dramatic increase in species diversity from the
origin of life to the present. But the patterns of species diversity are much more complex when
viewed in the fossil record. There are periods of rapid increase in diversity, periods of rapid loss
of diversity (mass extinction events) and subsequent periods of increased diversity. These
patterns beg a variety of questions about the dynamics of the history of species diversity and
what forces might regulate this diversity: are there equilibria of diversity?, does diversity
increase without limit?, are the patterns of diversity random patterns?
We will first consider some simple models of diversity. Two general processes that affect
standing diversity are origination and extinction. These processes are in turn going to depend
on the number of taxa, N present at any one time. Thus the change in the number of taxa per
unit time, dN/dt can be described as follows:
The rate of origination = O = # new taxa arising / existing taxon / unit time
The rate of extinction = E = probability of extinction during period dt.
thus, change in diversity = dN/dt = ON - EN = N(O-E)
Diversity will be constant if O = E, diversity will increase if O > E (speciation rates exceed
extinction rates) and decrease if O<E. Diversity might be maintained at a constant level if an
increase in O was matched with an increase in E: is there an equilibrium diversity? This could
only be achieved if there was some feedback between N, O and E to keep O and E in
approximate balance. Consider a graphical model where the equilibrium number of species
depends on the effect of N on the values of E and O (see figure).
These models just provide ways of thinking about the history of diversity on earth. What might
such diversity dependent forces/phenomena be? Do they exist?
What do the data tell us? First, how do we get the data? Simple on one hand: count the number
of taxa present in each time interval. Complicating issues: species concept = typological
(morphospecies) any "reasonably" different forms will be classified as a different species. If
these morphospecies co-occur in time and space then they are probably "good" species and
should be counted as separate entities. Many fossil series show temporal gradations of
morphology from one form into another. These chronospecies introduce error into estimates of
diversity since the end of one name and the beginning of another name look like extinction and
origination, or pseudoextinction and pseudoorigination. Moreover, the taxononic level under
consideration will alter one's estimate of the patterns of diversity since lower taxa (species,
genus) might vary in diversity more than higher taxa (family, order). Also, differences in the
identification of taxa will alter estimates of patterns (see figure 20.12, pg.577).

In the literature it is difficult to tell which extinction/speciation events represent real events and
not "chrono" events. We can avoid this problem by tabulating higher taxa. It is unlikely that all
representatives of a genus will evolve simultaneously into a new genus, but what is a genus (or
a family)? is it a real unit of diversity?
Additional biases in quantifying diversity: thickness of sediments different sediments deposit at
different rates so that the resolution is quite different among sediments (affecting the rate (dt)
component of the dN/dt calculations). Area of exposed sediments are not always representative
of the temporal and spatial scales one might want to sample/represent in a fossil assemblage.
Additional artifact of the age of the rocks known as "the pull of the recent" Young rocks are
less likely to be destroyed by the forces of time than are old rocks. This means that last
occurrences of a fossil are more likely to be better recorded than first appearances (actual first
"appearance" might have been exposed, eroded, reworked, etc. moving the observed first
appearance up in time). Thus the duration of lineages will be "pulled" toward the recent (pulled
implies an artifact of increased likelihood of a fossil to be recorded in younger rocks). Similarly,
and extant group with a single fossil occurrence has a temporal range from its fossil date
through to the present, but and extinct group with a single fossil occurrence has only that single
date as a temporal range, even if it lived for a long time but was not deposited as a fossil.
Biases aside, what does the record tell us? Does diversity increase with time? The Cambrian
Explosion ("sudden" appearance of many invertebrate phyla in the early Precambrian) shows a
clear patterns of increase in diversity from the known forms present in Pre-Cambrian strata.
Were there some physical triggers of diversity increase such as geologic activity inducing major
changes in the physical environment?. Or were there somebiological triggers that allowed the
rapid evolution of new forms? These might consist of the evolution of a key innovation (a
unique new trait that allows a species/taxon to exploit a new way of life)? This idea invokes the
concept of the adaptive zone, a new set of ecological niches utilized/exploited by a group of
related species in which this group might radiate (speciate) extensively and increase in diversity.
The diversity of marine invertebrates in the Phanerozoic (period of visible life) is the best
example. Increase from Cambrian to Ordovician, then mass extinction; increase to
plateau through the Paleozoic (major extinction events in middle of plateau); continuous
increase from Triassic through Tertiary (see figure below).
Patterns of increase of diversity indicate three evolutionary faunas: 1) Cambrian, 2) Paleozoic
and 3) Modern (work of J. Sepkoski). Despite the major patterns, different taxa have very
different profiles: there are examples of extinction and reradiation, maintenance of diversity
and continuous diversification all spanning the same time frame (compare fig. below with other
taxa: fig. 21.11 - 21.16. pp. 602-607). This suggests that if there are biological forces/pressures
regulating diversity, they may be acting quite differently in different taxa.
Increases in diversity were measured by Bambach in a slightly different way: he classified
organisms into guilds (groups of organisms with similar ways of life) and examined the increase
in taxonomic diversity from the perspective of guilds. Conclusion: increase in diversity through
the Phanerozoic achieved more by the increase in number of guilds rather than increasing
number of species within each guild. This suggests that"ecospace" becomes more tightly packed
through the Phanerozoic. Ecospace is represented by three axes and different species would "fill"
different regions of the "cube" of ecospace.

All these observations again beg the question: is diversity regulated, or put another way, can we
treat the patterns of diversity in the fossil record as we might treat an ecological system? There
are inferences that support both answers to this question. Computer models where the rates of
extinction and origination (speciation) fluctuated randomly. One constraint was that the
mean probability of a taxon going extinct equaled the mean probability of it speciating. Thus,
diversity would fluctuate but hover about some "equilibrium" value. Results produced patterns of
diversity within clades very similar to those observed in the fossil record (see below).
Data supporting the notion of regulation is the observation that rates of extinction and rates of
origination are correlated. This suggests that when speciation increases diversity, extinction
rates increase and bring diversity back down; similarly if extinction rates increased, speciation
rates would increase and bring diversity back up (beware of using a teleological argument; these
changes are effects of changes in diversity presumably occurring due to ecological pressures at
the time, not for the purpose of restoring diversity). Observation of correlation of extinction and
speciation rates suggest diversity dependent effects or feedback in an ecological sense.
Can also model patterns of increase in diversity as one would model exponential growth in
ecology N
t
= N
0
e
rt
where r = birth rate - death rate (or in our case, origination rate - extinction
rate). N
0
= 1 species (beginning of group) and t = time since first fossil
The data from Cambrian fit this relationship fairly well. Diversity during the Paleozoic fit
a Logistic growth curve quite well (logistic curve has a feedback where number if individuals
[taxa] levels off with increasing density; sigmoid curves in figure below)
One can extend this analogy even further and treat Sepkoski's three evolutionary faunas as one
might treat competing species. The patterns fit models of species competition. But: the
observation is a pattern in the fossil record and we do not know whether the process of
competition existed between the two major faunas. This pattern can be seen on a lower
taxonomic level also: rodents increase in diversity as the multituberculates(rodent-like
mammals) decrease to extinction. Shortly after the brachiopods (clam-like marine invertebrates)
bite the dust, the bivalves (e.g., clams) diversify extensively. The patterns look like what one
might expect fromcompetitive exclusion, and is referred to as ecological replacement since one
group with a similar set of key innovations replaces another group (see figure below).
Re analysis of the brachiopod/bivalve replacement has suggested that there has been no
interaction between the "competing" forms and that they are best though of as "ships that pass
in the night". This does not mean that all ecological replacements in the fossil record do not
involve competition, just that it is hard to say. A nice way to compare the possibility of
interaction, or the lack of it, is illustrated in figure 21.12, pg. 603.

MACROEVOLUTION: TEMPO AND MODE. I

We now consider the tempo (i.e., rate, and any modulation thereof) and the mode (i.e., the
particular form or manner) of evolution. The use of these two words to focus the study of
evolution is attributed to George Gaylord Simpson who's book, Tempo and Mode in Evolution,
brought a paleontological perspective into the Modern Synthesis and applied the thinking of
population variation and genetics the patterns of the fossil record. Thus, Simpson attempted to
show that macroevolution (evolution above the species level) could be accounted for by familiar
mechanisms of microevolution (genetic changes within population). He begins with the
question: "How fast, as a matter of fact, do animals evolve in nature?"
To answer this question we consider evolutionary rates. Simpson identified two general classes
of evolutionary rates: Phylogenetic (or morphological) rates measure the rates of evolution of
characters (single or complexes) within phylogenetic lineages and are quantified as
measured change in a character(s) per unit time; taxonomic rates measure the rates at which
taxa replace one another in the fossil record and are quantified by two reciprocal methods: 1)
number of taxa originating and going extinct during a span of time, or reciprocally 2) the average
number of years a taxon remains extant (more below).
Potential problems when taxonomy is based on morphology: high rate of morphological
evolution may lead to the division of organisms into many chronospecies. This can result in a
high rate of taxonomic evolution: withpseudoextinction and pseudoorignination, taxonomic
rates of evolution can be correlated with morphological rates of evolution (graph A). But, the
reverse (morphological rates correlated with taxonomic rates) will not necessarily hold in cases
where real extinction of taxa, and replacement by newly evolved taxa, occurs at a high rate. The
latter does not assume there is continuous change specific morphologies, thus we could have
high rates of turnover of taxa without extensive morphological change (graph B).

The relationship between morphological and taxonomic rates also depends on which characters
are used to determine taxonomic status. One character may evolve rapidly in a lineage but the
lineage may not be split into chrono "genera" because "important" characters have not changed,
i.e., there can be mosaic evolution.
Haldane proposed a unit of measure: 1 darwin = change by a factor of e per million years (e =
base of natural logs = 2.71828). See page 553 and figure 20.1, pg.554.
Horse teeth: 0.04 darwins = 4% per million years
Triceratops lineage of dinosaurs: 0.06 darwins
Rates appear to vary between different groups. There are apparent living fossils that have
changed very little, or not at all, in millions of years: the coelacanth, the horseshoe
crab (Limulus, see fig. 20.11, pg. 575) and the tadpole shrimp (Triops) are good examples. Other
species or groups have evolved relatively rapidly (Horses, see figure).
Rates of change also can vary during the evolution of a lineage. In lungfish a "score" was
tabulated for each taxon as to whether it possessed ancestral or derived traits. This score was
plotted against the age of the taxonomic group for which the score was tabulated. Resulting
graphs (See fig. 20.10, pg. 575) show a rapid loss of "primitive" characters (=acquisition of
"new" characters) through time and the slope of this curve shows a peak early in the lineage.
The point is that morphological rates of evolution can be very different in
both tempo and mode in different lineages of organisms.
Some of the between-group differences are real and some are an artifact of temporal scale.
Gingerich recorded rates of change in selection experiments, colonization events, post-
Pleistocene changes and long-term changes (domains I, II, III, IV in table figure below) and
plotted them against the measurement interval in years. The clear relationship indicates that
changes measured over short time spans exaggerate the changes one might predict if carried out
for a long time. There are reversals of morphological trends and periods of no change (="stasis";
next lecture) that reduce the rate of change when averaged over a long time period. See table and
fig. pp. 556-558.
Taxonomic rates can be quantified as number of genera / time span = average genera per
million years, or one can take the reciprocal of this and ask: How long does a genus last? and
thus quantify the duration of a taxon. By tabulating the period of first appearance of a taxon
(genus, lets say) and the period of its last appearance in the fossil record one can obtain such
taxonomic rates (see table below for example of data). In Pelecypod mollusks (bivalves) 13
genera appeared in the Ordovician and disappeared in the Ordovician; 4 genera appeared in the
Ordovician and disappeared in the Triassic. Compiled over the entire data set the "average"
genus of Pelecypod lasts 78 million years. Similar calculations for Carnivores show that in this
group a genus lasts about 8 million years. See data below and compare with fig. 20.13, pg. 578.
These data can be plotted on survivorship curves which tabulate the percent of taxa alive today
that originated at the time indicated on the horizontal axis (broken line). For extinct taxa the
graphs show the percent of taxa with a known duration > the value indicated on the horizontal
axis. Thus 100% of the extinct genera have a duration greater than or equal to 0 years and 0% of
the Pelecypod genera have a duration greater than or equal to 275 million years; other genera
have intermediate durations. Note the shorter range of the horizontal axis in the two graphs and
the different shapes of the extant vs. extinct survivorship curves in the two graphs.
The point is that the taxonomic rates of evolution can be very different in
both tempo and mode in different lineages. While the data are sound the interpretation of the data
as a general phenomenon holds to the extent that the unit of a genus is comparable in the two
lineages. Since the duration of genera in the two groups differs by about a factor of 10, this large
a difference suggests that there is a real difference. In other comparisons with more subtle
differences between lineages, the unit of measure (genus, family?) could become an important
consideration.

MACROEVOLUTION: TEMPO AND MODE. II

Niles Eldredge and Steven Gould stirred up the mud of Tempo and Mode in Evolution with their
paper in 1972 on so-called "punctuated equilibrium". The traditional view of evolution was one
of phyletic gradualism. This encompassed slow, gradual change in phenotype and speciation by
gradual change from one species into another. The alternative - punctuated equilibrium was put
forward as a means of accounting for the ever present"gaps" in the fossil record (see figs. 20.4-
20.5, pp. 561-562). Eldredge and Gould argued that the gaps were not artifacts of incomplete
representation, but that there were essentially no intermediate forms. The general notion is that
long periods of stasis or morphological equilibria are punctuated by periods of rapid
morphological change.
This issue was a bit of a blow to the traditional "Darwinian" approach to evolution which largely
focused on slow gradual change. This affiliation with "non-Darwinian" evolution is misguided
and mislabeled because the original and updated versions of punctuated equilibrium invoked
speciation in small isolated populations which fits squarely with Mayr's peripatric model of
speciation. Moreover, Darwin described in the Origin of Species a pattern that is entirely
consistent with stasis; Darwin did believe that the evolution of complex adaptations was gradual
(the eye was built adaptively from preexisting parts in ancestors and did not pop into being
quickly in evolutionary time).
The stratigraphic phenomena would be observed from 1) morphological stasis in a large
population 2) an unrecorded founder event to a peripherally isolated population 3) speciation,
perhaps through a "genetic revolution", where a new equilibrium morphology would be assumed
and 4) Range expansion of this new form back into the range of the original form (see diagram
below). These events, entirely consistent with "Darwinian" or "Modern Synthesis" phenomena,
would be observed as a punctuational pattern (see fig. below). Note that there are other
sequences of events that might give rise to the punctuational pattern.
Several questions arise:
1) What is rapid? 10,000 - 100,000 years can be an instant in geological time (especially in the
context of some deposition rates) but is ample time for evolutionary events in populations.
Recall that the shift from the peppered to the dark form of Biston betularia occured within the
span of 100 years by a completely "Darwinian" mechanism.
2) Is rapid morphological evolution associated with speciation events? Answer: not
always (many species of insects [lacewings, fruit flies] are "good species" but are very difficult
to tell apart). It can be: there are convincing examples of punctuated patterns in fossil
record: Williamson's mollusks.
3) How do we explain stasis? stabilizing selection, developmental constraints, absence of
selection? Eldredge and Gould claim that stasis is data, i.e., the absence of change is
interesting. If stasis is due to stabilizing selection, then there is perfectly good evolution going
on: selection against individuals at the tails of the distributions within populations. If stasis is due
to developmental constraints then there is an interesting "battle" going on between the
environment and the homeostasis of the organism. The issue of punctuated equilibrium has
contributed a lot to the science of paleontology since it has focused new attention on 1) changes
at speciation in the fossil record (see pp. 567-570), and 2) the notion that stasis is interesting and
important and needs explanation.
The publication of the idea of punctuated equilibria set off a bit of a challenge among
paleontologists to show that their "own" mode of evolution was the correct one.
Thus gradualists came out with papers showing convincing evidence of gradual evolution
(figure 20.7, pg. 565) and the Punc. Eq. types came out with papers showing rapid shifts in
phenotype in the fossil record. The absurd example is a data set by Gingerich which he interprets
as gradual and is reinterpreted by Gould and Eldredge as punctuational! (see below). Like any
polarized debate, there are two kinds of intermediates where reality lies: 1) some data sets show
one mode, others show the other and 2) documented cases of punctuated gradualism: periods
of stasis punctuated by short periods of gradual change. What remains to be confirmed is
whether different lineages tend to show one pattern and others the other: the relative
frequency of the two alternative modes in the fossil record will ultimately settle the debate.
The punctuation debated focused a lot of interest on the notion of hierarchical phenomena
(sensu units of selection). One important hierarchical issue is Species Selection: differential rates
of increase or decrease in species diversity among different lineages due to differences in rates of
speciation and/or extinction. The basic principles of species selection are 1) speciation is random
with respect to phenotype, 2) most changes occur at speciation, 3) different extinction and
speciation rates are due to some biological properties of the different taxa.
Some consequences: 1) species selection can introduce evolutionary trends and 2) differences in
morphological or taxonomic rates of evolution among different lineages can be due to species
selection. The important point is that it is the pattern of speciation that drives such trends, not
the direction of morphological changes.
An excellent example of the dynamics of species selection (or how one might interpret data from
the fossil record in light of differences in extinction and speciation rates) is provided by Hansen's
studies of planktotrophic vs. non-planktotrophic gastropod (snails). Planktotrophic lineages last
longer in the fossil record (lower extinction rate) See fig. 23.3, page 643. However, the
proportion of planktotrophs decreases in the fossil record (see figure 23.4, page 645 and note
typo in figure caption). How can one account for this apparent paradox? If one invokes a higher
speciation rate among non-planktotrophs, then this might do it; i.e., species selection might
account for the patterns of diversity changes. Read the text for this section (pp. 641-644).
A general question about species selection: is it a pattern or a process? Following the
parsimony of G. C. Williams, can we explain species selection by differential survival of
individuals within populations, and if so is species selection just a by-product of individual
selection., or do higher level processes operate? (thus the hierarchical issue in species
selection). If the latter is true, the big question remains: is macroevolutiondecoupled from
microevolution?? (i.e., are population-level processes insufficient to account for evolution above
the species level? If you talk to a population geneticist they would say NO! If you talk to a
paleontologistsome would say OBVIOUSLY!


EXTINCTION

Almost all professional football players are still alive. 4% of all human beings that have ever
lived are still alive. What percent of all species that have ever lived are still alive? 0.1%;
thus 99.9 % are extinct. Looking ahead, things look numerically bad for humans: chances are
that we will go extinct.
What is extinction? => Termination of a lineage. What are the units of extinction? Genus Family
? Do we determine extinction of a genus by the last remaining species that makes up that genus?
What happens if 99% of the genus goes extinct and one "hanger-on" last millions of more years?
No solution to the problem, these are the sorts of biases that are inherent in tabulating higher-
level phenomena.
What can we say about adaptation and extinction rates? is extinction due to: Bad luck or Bad
genes? (book by David Raup, W.W. Norton, Co.).
As to the causes of extinction here are some questions to "ask" the fossil record:
intrinsic/extrinsic: was extinction due to a characteristic of the organism (intrinsic) or of the
physical environment (extrinsic)? Was extinction due to competition (mutituberculates and
rodents) or was it due to major events like sea level changes or asteroid impact? One "asks" the
fossil record by looking at the data:
Taxonomic survivorship curves were tabulated by Van Valen, U. Chicago (see figure below).
Horizontal axis in the number of years that a group has survived (could be 50 Myr. in the
Cenozoic or 50 Myr. in the Paleozoic); vertical axis in the log of the number of taxa that
survived for the stated number of years. The ~ straight lines indicate that a constant proportion of
the taxa are becoming extinct at various stages of duration, which Van Valen interpreted to mean
that the probability of extinction is independent of age of taxon. This further implies that taxa are
not becoming better adapted (if one defines increased adaptedness as a decreasing probability of
going extinct). Note that these survivorship curves are different than the ones presented for
moluscs and carnivores. Note also that the graphs do not imply that there is a constant extinction
rate per unit time. The approximately linear relationship indicates that the taxa with a long
duration do not appear more resistant to extinction.
Van Valen proposed the Red Queen hypothesis to account for the pattern of approximately
linear survivorship curves. Van Valen hypothesized that 1) the environment is continually
deteriorating (~ changing so that current adapted state is no longer applicable), 2) organisms
have to adapt continually, i.e., you have to "run to stay in place" like the Red Queen said to
Alice in Through the Looking Glass (Alice in Wonderland).

Figure 22.3 from Evolution, 1st Ed.
There are other ways of looking at extinctions that contradict this idea. Extinction rates in the
Phanerozoic show a pattern of decrease in background extinction rate (see figure below;
"background" means excluding the five big peaks). Does this mean that species are becoming
more adapted because they are more resistant to extinction? The jury is still out (i.e., we don't
know). Moreover, some data sets show rates of extinction that vary dramatically over absolute
time, suggesting that extinction rates are not constant over time but vary widely. Compare figure
22.13, page 633. Once question is how much variation one tolerates before saying that extinction
rates are not approximately linear.
One interesting observation about extinction patterns is that a periodicity has been documented
in one data set. The cycle appears to be 26 million years. See figure 23.7, page 652.
Explanations for periodicity have been varied: Companion death star (Planet X out beyond
Pluto) cycling past earth every 26 million years which hurls asteroids at earth killing many taxa.
Needless to say, some of these ideas made astronomers HOWL with LAUGHTER.
Mass extinctions are quite a different type of extinction than the background extinctions. In
some regards mass extinctions rekindled ideas of Catastrophism (as opposed to
Uniformitarionism; see lecture 2). The impact extinction theory that mass extinctions were
indeed caused by asteroid (or other) impact is a good one because it falls into the mainstream of
scientific inquiry: an hypothesis that can be tested, and falsified, with further sampling or
experimentation (although conclusive proof that it did not happen may be difficult).
The Cretaceous-Tertiary (K/T ) Extinctions are some of the best studied. What went extinct?
marine reptiles, ammonites, dinosaurs, etc. However, many groups were relatively unaffected.
This presents an interesting problem: how could something that might be so devastating as to kill
off many diverse taxa be, at the same time, so selective with respect to different taxa? See figure
23.5, pg. 648.
The Alvarez's from Berkeley proposed that the K/T extinctions were caused by impact of a large
asteroid. Some compelling evidence supports the notion: Excess of iridium (iridium anomaly or
iridium "spike") at the K/T boundary (see fig. 23.6, pg. 649). This element is rare in earth's crust,
but not uncommon in meteorites. The presence of "shocked" quartz (likely to be formed at
asteroid impact, less likely to be formed by normal Earthly geological processes) is also in
excess at the K/T. Evidence for these diagnostic markers of impact have been sought at the other
"big five" mass extinctions and only one has any blip of excess iridium (no where near the spike
at the K/T).
There are some problems with the impact explanation: why was it so selective? and: where is
the impact crater? Well, sure, you know, ah, it, ah, it landed in the ocean! Or maybe it landed
near a subduction zone and the evidence has been conveniently tucked under some continental
plate. Also, there is evidence from magnetic reversals in the stratigraphic record that the K/T
transition is varies in time from place to place. Every couple of years someone publishes a paper
indicating that they found the impact crater; the most recent focus is somewhere near the
Yucatan peninsula or western Caribbean. Keep an eye on Nature and Science.
The issue of impact extinction puts all that we learned about population genetics and adaptation
in a very different perspective. So what if one allele is more fit than another, or the rate of
evolution depends on the amount of additive genetic variation in the population, if an asteroid is
going to blow us away tomorrow, then microevolution really is decoupled from
macroevolution. But what about those lineages that sail through the K/T boundary unaffected?
Maybe they were adapted, pre-adapted or just exapted for the impact and there is a coupling.

HUMAN EVOLUTION

Humans are too complex to be "understood" by any one field. Thus we will look at a few major
steps in evolution and some of the things affecting human evolution.
Humans are members of the order Primates which consists of about 180 species (there are 17
different orders of mammals which diverged 80-65 million years ago). Primates are a relatively
old order of mammals. Most of the synapomorphies of this order are associated with
an arboreal way of life: flexible digits, forward facing eyes, vision as a primary sense. These
traits may have played a role in the evolution of brain size in the lineage leading to humans.
Humans are a member of the family Hominidae which is believed to have diverged about 5
million years before the present (mybp) from the other members of the Old world monkeys. At
least 20 mybp the Hominoids split off from the other old world monkeys. The dates are rough
and get changed now and then.

Relationship of humans to African apes (= chimps, gorillas) and orangutan DNA hybridization
indicates that apes are our closest relatives. Human/chimp/gorilla relationships not proven but
chimps are most likely our closest relatives. The molecular clock says ~ 5 million years ago the
human-chimp line split.
While Chimp and gorilla have knuckle walking , the humans posses many traits associated
with bipedality: vertebral column, shape of pelvis, angle of femur, foramen magnum at base of
skull. Bipedality seems to be a major "innovation" which allowed humans to enter a new
"adaptive zone". The first human (Australopithecus afarensis) seems to have an angle between
the femur and tibia (Upper and lower leg) that is intermediate to that of humans and gorillas.
The evolution of modern humans from our hominid ancestor is commonly considered as having
involved four major steps: evolving terrestriality, bipedalism, a large brain (encephalization)
and civilization. There are (and have been) several competing hypotheses that have
acknowledged these four steps, but put them in a different sequence during human evolution.
Origin of Homo sapiens: Australopithecus afarensis = first bipedal hominid, found in east
Africa about 3.0-3.2 MYBP. Later forms became more slender (= "gracile"). Homo
habilis and H. erectus (~1.5mybp) came later. The evolution of bipedalism may have freed the
hands for us in other functions: carrying, tool use. The trends in the evolution of tool use (more
types, more specific tasks, different types of materials, more efficient use of materials) seems to
follow (lead??) the evolution of increase cranial capacity. These both seem to increase
noticeably about 2 mybp. One theme that involves each of the different sequences of evolution is
that there was some feedback that lead to the increase in cranial capacity, e.g., becoming bipedal
creates selection pressure for a more elaborate brain to control motor function and to process
incoming sensory information. This in turn would allow for more successful bipedalism, etc. The
same argument could be leveled about culture leading to an increase in brain size, and vice versa,
so the sequence cannot be resolved just on the logic of feedback loops alone.
Origin of "modern humans": Two alternative scenarios for origins: 1) humans originated in
more than one site ("Multiregional" model). Evidence supporting this are modern Homo
sapiens samples found in Asia and Africa 2) a single origin ("Noah's Ark" model: one origin
and dispersal out from site of origin). Homo sapiens are believed to have originated ~100,000 -
200,000 years ago.
Paleontological evidence suggests a single origin in Africa. Molecular data shows low genetic
diversity worldwide with the highest diversity in Africa, aslo suggsting an African origin. Recent
re-analyses shown that the cladograms of mtDNA cannot support an African origin on statistical
grounds. Moreover, some recent fossil finds have put humans outside Africa about 2.4 MYBP,
but these may be due to early migrations. However, three independent, recent articles in Nature
(March 31, 1994; vol. 368, pgs. 449-457) all support an African origin for humans; two are based
on fossil analyses and one is based on DNA analyses of microsatellites (next lecture).
The analysis of the evolution of culture and civilization in humans clearly must be based in
materials other than human bones alone. The evolution of tools is one reliable correlate (they are
recognizable as being rocks reworked as tools and, being rocks, they preserve well). The patterns
of tool form show some suggestive trends regarding civilization: through time more types of
tools become apparent and there is less variation among specimens in the shape/form of a
given tool (see figure). This has been interpreted as evidence for communication or "training",
since 'word may have spread' on just how to improve that stone ax so that it can be used more
effectively for certain tasks.
The spread of Homo out of Africa is presumed to have taken place about 1.5 MYBP by Homo
erectus. This species seems to be on a trajectory of brain size and body size that
looks anagenetic, whereas one lineage that lead to Australopithecus robustus seems to be on
another line. In a broad sweep of time, the notion of the chimp leading to the Australopithecine,
to Homo, to the Neanderthal to the modern American family standing in their driveway is a
myth. There were lineages that diverged in a branching cladogram, some of which did not make
it to the present. Evidence for this is provided by more than one distinct morphological type of
early humans present at the same time (see below). As time gets closer to modern humans,
however (Homo erectus on up), a phyletic gradualist anagenesis is more easy to accept.
Once a big brain is achieved and this provides the intellect for an organism to anticipate its
environment, the notion that an organism evolves in response to changes of the environment
becomes too simplistic. Humans evolved the power to alter their environment so as to protect
themselves from its abiotic pressures. This means that they are altering their own selective
pressures and a dialectic emerges between the organism and the environment such that these
cannot be separated. Other organisms do this (beaver dams, deciduous trees), but in humans this
cycle is accelerating. The rest is history.

HUMAN DIVERSITY

Modes of evolution Throughout course we have stressed that traits must have a genetic basis
WHY? for transmission to next generation. What do humans have that allows transmission to
next generation without genetics?? CULTURAL transmission. This is a major distinction with
other animals (although other animals do have "culture", it is not as "advanced" as humans)
Cultural transmission can be vertical (between generations) or horizontal (within generation).
Vertical cultural transmission is Lamarkian: what you acquire during your lifetime you can pass
on to your offspring ("inheritance of acquired characteristics").
Some analogies with other evolutionary forces:
- mutation ~ innovation, new behavior, skate boarding, rap music, pierced navels
- selection ~ popularity, status: trait gets swept into high frequency
- drift ~ random variation in culture, language, dialects (southerners, Maine hicks, etc.)
- there can even be gene flow: yo!, like dude, my cousin in California pierced her navel!
Communication, and especially language, are further "key innovations" that may have lead
humans into a new "adaptive zone". But literature (Lascaux cave paintings, National Inquirer;
and now consider electronic transfer of literary info, e-mail, etc.) really sets us apart. Our rate of
evolution is dramatic on all counts. While the beaver, in building its dam, alters the environment
that surrounds it, it has evolved in this context of altering its environment in a predictable way
for a long time. We are no where near "equilibrium" with respect to how we are evolving with
the extensive alterations we are making to our environment. One hopes that we have the genetic
wherewithal to "run fast enough just to stay in place" (as the Red Queen suggests we must).
All organisms vary and humans are quite good at recognizing nodes or clusters in that variation
(demes, populations, species). The nodes or clusters within human phenotypic variation are quite
pronounced and most of us would sort the ambassadors to the UN into more-or-less the same
"groups". The question thus arises: how is the genetic variation within humans partitioned? This
question was asked (and answered) by R. C. Lewontin in 1972 (The apportionment of human
diversity. Evolutionary Biology vol. 6: pp. 381-398).
Lewontin collected data on the frequencies of different alleles at various nuclear loci in different
human populations. These populations were nested into larger groups we know as races, and the
various races can be nested further into the larger group we call the species Homo sapiens.

With data on allele frequencies in each population, Lewontin could ask how much additional
variation is added to the unit in question by pooling together the data from all populations within
races, or at one level up the hierarchy, by pooling all the data from within races to one large
species sample.
To quantify what proportion of the total genetic variation within humans, a measure of
"heterozygosity" was used similar to H = 2pq (or [1- (allele frequency
i
)
2
] for i different alleles;
in the paper the very similar Shannon-Weaver index was used). The numbers obtained from this
formula provide a measure of genetic diversity at each of the many loci tabulated by Lewontin.
Four points are relevant in thinking about this measure of "diversity": 1) a locus with only one
allele will have H = 0; 2) the greatest diversity will be when all alleles are equally frequent
(p=q=0.5 for 2 alleles; p
1
=p
2
=p
3
=p
4
=0.25 for 4 alleles); 3) diversity will increase as the number
of alleles increases (the 4 allele case above is more 'diverse' than the 2 allele case); 4) diversity is
a convex function of allele frequency (a diversity measure from a pooled sample obtained by
combining alleles from two different populations will be greater than the average of the two
diversity measures from each population).
These H values can be tabulated for several different levels of the hierarchy described above: by
considering a single population's p and q, or the average p and average q within a single race
(averaged among all populations within that race = H
pop
), or the average p and average q for all
races (pooling all populations within a race to determine the p for that race, then averaging the
p's for each of the races = H
race
). H
species
will be determined by pooling all populations irrespective
of race to obtain a species-wide p, then calculating H = 2pq (or as above for the multiple allele
case). Thus we can have an H
pop
which will be less than H
race
which, in turn, will be less than
H
species
.
These H values can then be partitioned or apportioned so that the total variation within humans
can be attributed to the within population component or to the within race component or to
the between race component. The simple expressions for these, and the data for each locus are
presented below. The conclusions from the results are very clear. Of all the variation within
humans, 85.4% of it lies within populations (i.e. is due to variation among individuals within
populations). An additional 8.3% lies between populations within races. Only 6.3% of all the
genetic variation within humans is due to differences between races!
Recent analyses with microsatellites in human populations give slightly different numbers, but
the general conclusions are the same. Microsatellites are regions of the genome that generally
show a repetition of a simple sequence, such as CA repeated over and over. In some instances
the repeated units can be longer and these regions are called minisatellites. See figs. 10.9, 10.10,
pg. 271-272 for an example. Such regions are very useful since the repeated sequence allows for
the insertion and deletion of repeats. As a result, there can be many alleles in a population that
differ in the number of repeated units in the specific region of the chromosome. This allows for
the discrimination among individuals, based on whether they share, or do not share, alleles of
similar length. This is determined by amplifying a person's DNA using specific primers in a PCR
reaction, and running the two samples out on a gel. If bands are shared, the two individuals are
related, if the band sizes do not match, the two are unrelated (or if you are an accused criminal,
you might be convicted or let off the hook based on these sorts of DNA 'fingerprint' analyses).
As with protein allele frequencies, one can still calculate the H values described above and
partition the variation into different levels of a hierarchy.
Lewontin concludes that there is no genetic or taxonomic basis to racial distinction and
classifications of this sort are of no social value. While you are free to agree or disagree with
Lewontin's social interpretation of the data, the population genetic conclusions are clear: with the
largest component due to variation among individuals within populations, each and every one of
us matters.