Hybrid Origins of Plant Species

Hybrid Origins of Plant Species Author(s): Loren H. Rieseberg Source: Annual Review of Ecology and Systematics, Vol.
28 (1997), pp. 359-389 Published by: Annual Reviews Stable URL: http://www.jstor.org/stable/2952498 . Accessed: 26/10/2011 12:39
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1997. 28:359-89 Annu.Rev.Ecol. Syst. Reviews Inc. All rights reserved right 1997 byAnnual Copy
HYBRID ORIGINS OF PLANT SPECIES

LorenH. Rieseberg
47405; Bloomington, Indiana Indiana University, BiologyDepartment, e-mail:lriesebe@bio.indiana.edu
KEY WORDS: speciation reproductive isolation, hybridization, introgression, plants,
ABSTRACT is theoretically difficult beof speciesviahybridization Theorigin newhomoploid in Nonetheisolation sympatry. the of causeitrequires development reproductive for used bybotanists account theforto and less, thismodeis often carelessly to intermediate respect related with are mation speciesthat morphologically of of and studies theoretical, empirical experimental, congeners.Here,I review of and the tempo, frequency speciation evaluate feasibility, to homoploid hybrid and syntheses thismode. Theoretical simulation studies, experimental models, evolutionalthough of stabilized thatit is feasible, hybrid neospeciesindicate to by appears be promoted rapid are Hybrid speciation aryconditions stringent. A of habitat. selfing and hybrid chromosomal evolution theavailability a suitable but advantage establishmenthybrid of species, this may breeding system enhance selfrates natural of among hybridization to by appears be counterbalanced lower that experiments suggest hybrid also studies crossing and ingtaxa. Simulation beobserved can confirmed thecongruence by speciation be rapid-a prediction of and hybrid species.The hybrids ancient tween genomes early the generation in have natural examples plants of frequency thismodeis less clear.Onlyeight that hybridizabeenrigorously documented, suggesting itmaybe rare.However, and in may populations, hybridization be tion rates highest smallorperipheral are envisioned or reorganization as for important a stimulus thegenetic chromosomal in founder effect saltational and modelsofspeciation.
INTRODUCTION
consequences, includingincrease mayhave severalevolutionary Hybridization of (2), intraspecific geneticdiversity theoriginand transfer geneticadaptation
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(2,93), theorigin newecotypes species(42, 102),andthereinforcement of or orbreakdown reproductive of barriers 55,77). Although frequency (27, the and a importance theseoutcomes notyetclearin either of are plantsor animals, critical bodyof datais now availableforassessing mechanistic the basis and frequency one ofthese-theorigin newspecies.The lastcomprehensive of of review thistopicin relation plants of to was Grant's (42) monograph "Plant of listedsix mechanisms whichthebreeding behavior Speciation."Grant by the for thus couldbe stabilized, providing potential speciation: hybrids 1. asexualreproduction; 2. permanent translocation heterozygosity; 3. permanent polyploidy; odd 4. allopolyploidy; 5. thestabilization a rarehybrid of segregate isolated postmating by barriers; 6. thestabilization a rarehybrid of isolated premating barriers. segregate by The first three thesemechanisms of of generate flocks clonaloruniparental the thatspan the rangeof morphological microspecies variability between is or parental species. Sexual reproduction amongmicrospecies limited abin it to sent,making difficult discusstheir origin and evolution thecontext of sexualisolation and speciation.By contrast, latter the three mechanisms generate sexualderivatives therefore thepotential giveriseto new and have to biological species. Thisreview focuses theorigin sexual, on of homoploid hybrid species(mechin of anisms5 and 6), (butsee 50,89 forreviews polyploidy plants). After unclarification concepts terminology, historical of the basisofourcurrent and of Thisis followed examination derstanding hybrid speciation reviewed. is by of thefrequency natural and of of hybridization an exploration experimental of andtheoretical studies test feasibility homoploid that the hybrid speciation. has I Once thefeasibility thismodeof speciation beenestablished, briefly of the used foridentifying critique methods homoploid hybrid speciesin nature that focus those on of andthen examples hybrid speciation arewellestablished. Finally, discusspromising I areasforfuture research possibleapproaches and that of mayfacilitate studies this mode.
WHATIS A HYBRID SPECIES?

Both"hybrid" "species"can have severalmeanings evolutionary for biand to formed crosscan ologists. The term hybrid be restricted organisms by fertilization more between of individuals different species,oritcan be defined
HYBRID PLANT SPECIES
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are "which disfrom populations individuals between as broadly theoffspring this characters" (44). I prefer heritable on tinguishable thebasisofoneormore in flexibilityusage. Nonethegreater as of broader definitionhybrids, itprovides species. between formed crosses by review, focuson hybrids I less,in this confrom of ranging variety definitions, Theterm specieshas a muchwider descent. to to ceptsbased on theability interbreed thosebased on common Mayr's(59) biologicalspecies concept-"speciesare groupsof interbreedsuch all from other isolated whichare reproductively populations ingnatural I of accepted these.Althoughhavepreviwidely the groups"-is perhaps most (73), itsemphasis of concept the concern about limitations this ously expressed to of a approach thestudy isolation does offer straightforward on reproductive is barriers particularly of the (20). Moreover, evolution reproductive speciation the species;otherwise, newhyof origin newhybrid crucial thesuccessful to its Thus,thefocus by bridlineagewillbe swamped geneflowwith parents. new isolation between hybrid is of review on theevolution reproductive ofthis parents. and lineages their
HISTORICAL PERSPECTIVE
appearsto have that The hypothesis newspeciesmayarisevia hybridization to "it in 84), whowrote is impossible doubt with (58; cited originated Linnaeus it generation.... For thence hybrid by thatthere new speciesproduced are themanyspeciesof plantsin thesame genusin the that appearsto follow, from than and couldnothavebeenotherwise oneplant, havearisen beginning view of This representsmodification theorthodox a thishybrid generation." by specieswerecreated the that which asserted all existing ofspecialcreation, (15). However, hybrids of the denied existence constant handofGodandwhich of and to werelimited F1 hybrids, he was unaware Linnaeus'observations and such with difficulties hishypothesis as segregation sterility. potential was by of hybridization initiated Joseph study plant experimental Rigorous found Kolreuter (84). First, in discoveries Kolreuter 1760andledtotwocritical no produced seeds-the from Nicotiana paniculata x N. rustica that hybrid a are that plants concluded hybrid Kolreuter first mule."As a result, "botanical in to and difficulty areunlikely occurinnature theabsence onlywith produced and to or intervention disturbance thehabitat.Second,Kolreuter of human to tended hybrids that generation discovered later his successor, Carl Gartner, of hythe thusrefuting existence constant revert to theparental forms, back viewofspecialcreation (84). The viewsof the brids supporting orthodox and not of (although necon Koireuter Gartner thelack of constancy hybrids and botanical hybridizers prominent heldbymostother on were essarily creation) John Charles Darwin, including the and centuries, during eighteenth nineteenth
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Mendel,CharlesNaudin,and Gregor Shireff, Goss, ThomasLaxton,Patrick WO Focke (84). to continued arise. For instance, hybrids of reports constant Nonetheless, themselves preserve sometimes ofplants varieties that Herbert noted hybrid (49) were controversial, although as almostas distinctly species. These reports, suchas Mendel(61), whoemphasized botanists by seriously prominent taken to evolutionary importance the is paper:"Thisfeature ofparticular inhisPisum of attain status newspecies" the hybrids becauseconstant history plants, of that the Naudin(66) also recognized possibility in (emphasis theoriginal). in latergenerations thatthismay and may becomefixed characters hybrid of recognition explicit the Thisrepresented first speciesformation. facilitate and thus maybecomestabilized hybrids that thepossibility later-generation speciation. modelsofhybrid modern foreshadowed was in role of hybridization speciesformation takena step The potential role the (51), who recognized important of habitat further AntonKerner by hyalthough realizedthat Kerner speciesestablishment. in governing hybrid required establishment their in successful werefrequently formed nature, brids species. Thiswas that suitable openhabitat was notoccupiedbytheparental role playsan important in as a significant contribution,ecologicaldivergence his Kerner restricted discussion However, current of speciation. models hybrid associatedwithmany the problems thus to fertile hybrids, ignoring sterility the failedto recognize potential Kerner like Furthermore, Linnaeus, hybrids. in of the of and problem segregation, itwasnotuntil rediscovery Mendel'swork of that speciof century theold problem hybrid theearly portion thetwentieth a is by correctly-what themechanism which newfertile ation couldbe stated isolated and constant lineagecould arise and becomereproductively hybrid from parents? its was made by Winge(103), to The first majorcontribution thisproblem inspeciescouldbe derived hybrid that and whopostulated a fertile constant chromosome (i.e. complement of stantaneously theduplication a hybrid's by in confirmed was experimentally a This hypothesis quickly allopolyploidy). to is and of species, allopolyploidy nowrecognized be a prominent variety plant in and (89,93). modeofspeciation flowering plants ferns in of speciation theabsenceof ploidal the By contrast, feasibility hybrid (65). He posuntil was addressed Muntzing it by unsolved changeremained inlater-generation hyof rearrangements that tulated thesorting chromosomal that of lead to theformation newpopulation systems bridscould,by chance, factors of sterility for werehomozygous a uniquecombination chromosomal wouldbe fertile, stable,and at the population (Figure1). The new hybrid from both isolated reproductively sameploidallevelas itsparents, partially yet authors barrier. Although early sterility speciesduetoa chromosomal parental
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1Xi
Species-1
1111
Species-2
Fl
gametes,/
Novelbalanced
Novel F2homozygotes
The of speciation. two the stages recombinational modelfor initial Figure1 Simplechromosomal number = 8), butdiffer tworeciprocal by (2n specieshavethesamediploidchromosome parental chromosomal for will be heterozygous the parental The first hybrid generation translocations. to classes of gameteswithrespect chromosome and rearrangements will generate16 different inviable todeletions due and willbe unbalanced presumably structure shown).Twelveofthese (not will recover The remaining will be balancedand viable. Two of thefour four and/or insertions. If two the karyotypes. selfed, whereas final willhaverecombinant structures, chromosome parental TheseF2s that will of a smallfraction F2 individuals be recovered possessa novelhomokaryotype. with intersterile theparental species. will be fertile stablebutwillbe at leastpartially and
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on the of (33,65), itis clearthat sorting focused chromosomal rearrangements modelsingenerate similar results. Thus,current genicsterility factors should contributions sterility factors. Modern corporate genicandchromosomal both (39), include termed recombinational speciation to thestudy thisprocess, of tests rigorous experimental theoretical ofthemodelas wellas thegradual and case from nature. accumulation well-documented studies of speciation model with of Concomitant thedevelopment therecombinational that speciesmight becomeisolated was thegrowing recognition new hybrid or barriers rather hybrid than sterility inviability. from parents premating their by of in of origin In fact, viewwas implicit Kerner's this (51) account thehybrid to isolated from parents its which Rhodendron intermedium, appears bepartially Grant Morerecently, (38) and behavior pollinators. of duetosoilpreferences the in basedon flower a speciation flowering plants presentedmodelfor sympatric thathybridization be of and might as constancy pollinators thensuggested for in structures the required speciation. likely mutation generating newfloral as of or studies thishypothesis Unfortunately, rigorous experimental theoretical have have notbeen conducted.Nonetheless, number empirical a of studies alone,and new barriers identified hybrid taxa thatare isolatedby premating the species by isolatedfrom parental recombinational species are typically and bothpremating postmating barriers.
THE FREQUENCY OF INTERSPECIFIC HYBRIDIZATION

and comData on naturally are hybrids quiteextensive, several occurring plant in the comof Perhaps most pilations illustrate extent hybridizationnature. the of examples is (52) compilation 23,675putative prehensive listing Knobloch's with ofinterspecificintergeneric or but must interpreted hybrids, this figure be and known hybrids Some ofthehybrids appearto be fanciful, many caution. and havebeenomitted Knobloch included natural artificial both (92). Moreover, natural hybrids. and fraction this of listing comprises hybrids, itis not clearwhat A morereliableindicator the frequency hybridization comes from of of a recent of reviewof fivebiosystematic floras (28). The frequency natural ranged from when to number speciesintheflora of hybrids compared thetotal flora theBritish flora 5.8% for intermountain of to the approximately for 22% a North with average 11% overall five an of floras. Assuming similar America, total ofnatural worldwide, wouldsuggest worldwide this a frequency hybrids of 27,500 hybrid plantspecies. amongthe250,000 described combinations a this it underestimate; Although is a sizablenumber, mayrepresentsubstantial to havegoneundetected to inadequate attention due systematic many hybrids in certain certain floras. groups
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Natural also hybrids werefound be unevenly to distributed taxonomically (28). Only16%-34% ofplant families 6% -16% ofgenera and haveoneormore reported hybrids. Thus,contemporary hybridization notbe as common may or ubiquitous believed, appearsto be concentrated a smallfraction as but in of families genera. Notably, life-history and the characteristics significantly associated with thesehybridizing genera include perennial habit, outcrossing and breeding systems, asexualreproductive modesthat allow stabilization of hybrid reproduction. The estimates provided aboveindicate therateofnatural that hybrid formationin plants sufficiently to provide is high for ampleopportunity homoploid hybrid speciation. Although hybrid speciation seemsmostlikely be importo in or tant family generawithhighratesof contemporary even hybridization, rare hybridization events be evolutionarily can important, a single, as partially fertile, hybrid individual suffice theprogenitor a new evolutionary can as of lineage(28).
THEORY
Models
is Homoploid hybrid speciation unusual becausenotonlydoes it involve hybridization taxaat thesameploidallevel,butitalso representstype a between of sympatric as co-occur speciation, theparental speciesmust geographically to produce hybrids. Chromosomal modelsforthisprocesswereproposed by as Stebbins (94) andGrant (39) andcan be summarized follows (Figure1): 1. Two parental speciesare distinguished twoor moreseparable by chromosomalrearrangements. 2. Their sterile and partially hybrid givesrisevia segregation recombination to newhomozygous recombinant for rearrangements. types the 3. Therecombinant arefertile within linebutat leastpartially the sterile types with both parents. in Grant the of (39) also notedthat formation newstructural homozygotes theprogeny a hybrid morelikelyunderconditions inbreeding of is of than of outbreeding. This leads to theprediction recombinational that speciation should morecommon selfing in outcrossers. be speciesthan A moregeneral modelhas recently beenproposed Templeton that by (98) and and the incorporates chromosomal genicincompatibility recognizes both important of selection ecologicaldivergence. roles and this Moreover, model canbe applied the to stabilization hybrid of isolated either segregates by prematTherearefour critical model: ingorpostmating barriers. stepsin Templeton's
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due by and breakdown tochro1. Hybridizationfollowed inbreeding hybrid is mosomal genicincompatibilities. or are by 2. Hybrid withthehighest fertility viability favored seor segregates who from modelofGrant Stebbins, emphasized the & lection. (Thisdiffers novelhomokaryotypes). theroleofchancein generating reproductively if 3. A newhybrid genotype becomestabilized itbecomes may from parental species. Otherwise, willbe overcome gene it isolated the by isolation will evolveas a flowwithitsparents.Presumably, reproductive or rather thanby of for viability fertility, by-product selection increased see for rearrangements (although 86). selection particular chromosomal withone or 4. Once a hybrid becomesstabilized, mustco-exist it genotype or outcome bothparents occupya new ecologicalniche. Either requires ecological divergence. this that Templeton emphasized factors appeartofacilitate mode.First, two the hyof barriers between stabilized he argues theevolution reproductive that chromosomal evolubrid and couldbe facilitated rapid by genotype itsparents of ina population rearrangements segregating tion. presence chromosomal The if canleadtofurther chromosomal breakage 86),particularlyaccompanied (81, there substantial is evidence genicmutation that byinbreeding Moreover, (56). and ratesalso increase hybrid in chromosomal populations (13). The elevated rates hybrid in are referred as hybrid to dyspopulations often genicmutation in and than exception hybrid the genesis, it nowappearsto be therulerather evolution shouldalso be enhanced populations (13). The rateofchromosomal willreduce effective subdivision becauseboth and/or byinbreeding population of chromosomal rearrangements sizesandincrease fixation novel the population drift. through of A secondfactor Templeton even critical rates speto that considered more of ciation thismodeis theavailability suitable via of habitat. The importance for was recognized and habitat theestablishment successofhybrids previously roleof commented thecritical on (2). Kerner by Kerner (51) and Anderson for establishmenthybrids, of whereas Anderson emphasized "openhabitats" the of theimportance habitat for of disturbance facilitating breakdown premating and propreviously isolated parental species, for reproductive barriers between which often diverge ecologically suitable for segregates, viding habitat hybrid in in from bothparents Moreover, is discussed detaillater thisreview, as (2). relative to in that most bonafide hybrid speciesarefound habitats areextreme a theparental roleforhabitat availability species(71, 100), implying critical in hybrid speciation. andecologicaldivergence homoploid
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Simulation Studies
of study thefeasibility dynamics hybrid of and The onlydetailed quantitative on chromosomal was et speciation byMcCarthy al (60) whofocused thestrict or recombinational modelandused computer simulations testhowvarious to of species and parameters affect rates establishment spread recombinational of in The simulated breeding a hybrid ina spatially structured environment. model nonoverlapping discreet plant zone between hermaphroditic specieswith two of and were The parameters tested: generations no seed dormancy. effects five (c) rate, of fitnesses stabilized of derivatives, selfing (a) fertilityFls, (b) relative species,and (e) of differences between parental the (d) number chromosomal of (thisparameter increases number hybrid the hybrid zone interface length matings generation). per with Most of thefindings wereintuitive consistent thesimplegenetic and the was facilitated (94). In general, process modelsofGrant (39) andStebbins for types, F1 a advantage recombinant by increased fertility,greatselective of differences between the highselfing rates,a smallnumber chromosomal recombinational zone interface. However, parental species,and a longhybrid as the was F1 speciation possibleevenwith fertilities low as 0.018, although for number generations of required the new species to becomeestablished but retarded speciation the process, givena was high. Likewise, outcrossing derivatives = 2.0), for (a advantage thestabilized sufficiently selective high of theprocessbecamefeasibleeven underconditions obligateoutcrossing. of the numbers Similarly, processwas slowedbutnotruledoutby increased the differentiating parental species or a short chromosomal rearrangements hybrid zone interface. of In addition establishing feasibility therecombinational to the speciation of the several newinsights thedynamics into model, simulations revealed also was theprocess. In particular, longperiods speciation "punctuated": hybrid in the ofhybrid transitions which selected zonestasiswerefollowed abrupt by the became established rapidly and displaced parental species.Apparently, type of in of thecritical factor thisprocessis thenumber individuals theoptimal are are numbers low. of own recombinant as mates their kind scarcewhen type, of leads type Thisleadsto a feedback effect increased as numbers theoptimal increases the to an increased chanceof finding similar a mate,whichin turn in and number optimal of generation, so forth. types thenext it of of Giventhecritical effect the number optimal typeindividuals, is is of not that perhaps surprising thespatialdistribution theseindividuals also are that individuals are clumped more important. Optimal recombinant-type that to thosethat evenly are high dispersed. Thus,it appears likely matethan facilitate mode. this but rates should selfing low dispersal
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An important parameter thismodelis therelative in fitnesses thenew of recombinant types. To implement selection their in model,thehomoploid derivative assumedto havea new,better-adapted was of hybrid combination in overall other and genes, resulting a selective advantage types (both hybrids parentals). Although increasing an number studies of suggest a subset that of the in hybrid genotypes be more than parental may fit genotypes certain habitats in of (reviewed 7), nonehas measured lifetime fitness. Thus,thevalidity this is would assumption untested. Also,itseemsunlikely thehybrid that genotypes be morefit in than parentals all habitats thehybrid the in zone. However, the occurrence newhybrid of in neither can speciesinhabitats which parent survive than (103) does suggest particular that hybrid genotypes be morefit may their in parents novelhabitats below). (see
Other Considerations
All ofthese discussions haveassumed theestablishmentthenovel that of hybrid will in type occur sympatry both with parents. Although hybrid speciation must in be initiated sympatry, Charlesworth argued this (18) that modeis most likely when"a group hybrid of plants colonizea newlocality arebychancespaand or founder tially ecologically isolated from parental the species."Thus,hybrid events that might viewedas foci of speciation.The possibility a hybrid be derivative might stabilized parapatry allopatry be in or shouldnotbe seen as of barriers. the As minimizing importance thedevelopment reproductive the of derivative becomes established expands geographic and its hybrid distribution, itmostlikely comebackincontact will with parents. its Presumably, existhe tence reproductive of barriers allowittosurvive challenge sympatry. will the of Thesimilarity homoploid of hybrid speciation saltational andfounder to (56) beenrecognized 71). effect modelsof speciation 59) has previously (16, (37, be Rieseberg (71) suggested intra- interspecific that or hybridization might a stimulus thechromosomal for envisioned Lewis's saltational repatterning by model.Similarly, that is Grant Grant & (37) argued hybridizationmorelikely than in founder events generate genetic to the reorganization proposed founder effect models. Theoretical that events provide to studies indicate forfounder must contain significant isolation, founding populations highlevelsofgenetic with to selection load, whichis subject strong epistatic (12,98). Populations thesecharacteristics instantaneously created hybridization are by (79). The small, in and peripheral populations emphasized thesaltational founder modelsalso arethosemost In the the proneto hybridization. general, smaller of the the population larger relative proportion foreign pollen, seeds,orspores in becausepollinators time (27). Moreover, spendmore periods foraging large thansmallpopulations, proportion interpopulational presumably of and the also in interspecific matings increases thelatter (27). Peripheral populations are
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because propagules reproductive levelsof foreign higher likely experience to at matesis likelyto be greater the interspecific of theproportion potential for support additional provide of boundary a speciesrange.Theseobservations in events speciation. founder role hybrid an important for
ESTIMATES OF HYBRID FITNESS

of the in occurs sympatry, fitness thenewhybrid speciation hybrid Ifhomoploid either fit is lineage more than role.Ifthenewhybrid playa critical lineage must et in as in parent all habitats, assumed theMcCarthy al (60) model,itquickly of if advantage thehybrid species. However, thefitness replacestheparental (98) as habitat, assumedin Templeton's to lineageis restricted a divergent if species. Finally, the new model,thenit mustco-existwiththeparental it be habitats, cannot and in lineageis less fit bothparental divergent hybrid in maintained sympatry. events, founder in critical hybrid be should less immediately fitness Hybrid speciesis rewith for as thepotential geneflowor competition theparental to the lineageis likely expand onceestablished, newhybrid duced. However, both point, species.Atthis with parental the itsrange comebackincontact and lineagecould as and becomecritical thehybrid isolation fitness reproductive or geneflow competition. be eliminated either by of stabilized fitnesses fertile, the concern with average is Notethat primary the fitness classes.Nonetheless, hybrid segregating not lineages, Fls orearly hybrid into insights thelikelihood can hybrids provide estimates earlygeneration of expectations possiblefitness and speciation can suggest of homoploid hybrid the between It derivatives. also is usefulto distinguish forstabilized hybrid of and class ofhybrids thefitnesses particular fitness a genealogical of average as Finally, has beenstressed communication). personal (V genotypes Grant, must recognized. and be between habitat fitness (5), byArnold theinteraction (e.g. F2s, of generations and The averageviability fertility earlyhybrid speciesdue to the to F3s,etc) is predicted be lowerthanthatof theparental whatis found, of (24). Thisis generally genecombinations break-up adaptive barriers.Wellreproductive postmating for particularly specieswithstrong Zauschneria (19), Layia (19), Gilia (40), and include characterized examples if specieswouldmerge Helianthus (45). Thismakessensebecausehybridizing The than of weregreater that theparents. fact fitness thehybrids of theaverage are that in also zonesarelimited extent implies hybrids on that most hybrid plant a habitats. Although their less than (21), at leastinparental parents average fit of of the havedescribed replacement populations rare studies of number recent to swamping swarms 55,77), this appears be duetogenetic taxabyhybrid (14, fitness. rather highaverage than a numerically hybrid congener larger by
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of fitness the in examples which average are there several hand, On theother to to appears be equivalent orto exceed class a particular orclassesofhybrids (reviewed measured parameters at parents, leastforthosefitness that their of stableand weremoredevelopmentally hybrids Artemisia in 7). Forexample, (31,35), and Iris (29) parent ratesthaneither seed germination had higher parents ratesthantheir growth vegetative had and Oryza(53) hybrids higher measured none Unfortunately, of thesestudies habitats. or in parental hybrid rule to valid they so fitness, whether represent exceptions thegeneral of lifetime fitness hybrid enhanced Nonetheless, is fitness unclear. hybrid average reduced are barriers weakandthehybrids isolating if does seemplausible postmating change(2, 36). conditions (30, a occupy novelhabitat 63), orifenvironmental fitness so plant in are Theseconditions common hybridizing species, rank-order not should be unexpected. hybrids favor that estimates occasionally of is generation lowerthanthat the of fitness a hybrid Even iftheaverage hythat species,thisdoes notrule out thepossibility a particular parental in particularly novelor parent, be might morefitthaneither bridgenotype are estimates notyetavailable fitness lifetime habitats.Although "hybrid" hybrid that is evidence accumulating particular indirect hybrids, for individual For habitats. example, in parents hybrid their than may genotypes be morefit swarms for reported hybrid are associations often genotype-habitat significant accrues advantage thata selective this (2,23,68,95). Presumably, indicates these although habitats, in whenfound favorable genotypes forcertain hybrid that studies factors (16). Likewise, historical from correlations couldalso result invarialmost in parameters hybrids fitness or viability, other fertility, describe fit that of genotypes aremore of the ablyreport presence a smallfraction hybrid fitness reduced exhibit on even than individuals, ifthehybrids average parental that which studies suggest by are (40,45). Theseobservations supported genetic hybrids, in may a small of fraction genecombinations be favorable interspecific peaks.For adaptive unoccupied to them colonizepreviously allowing perhaps interspein tested sunflower gene interspecific combinations 5% instance, ofthe of speciesin the werefavorable (79). Finally, occurrence hybrid cific hybrids that (71) can parent survive does suggest assumptions neither in habitats which are in of genotypes novelhabitats realistic. hybrid ofgreater fitness certain
EXPERIMENTAL STUDIES of VerificationtheRecombinational Experimental Model Speciation
have focusedon speciation hybrid studiesof homoploid Most experimental between hybridization recombinant typesfollowing the recovery fertile of
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earlystudyin thegenus parents. A relevant chromosomally differentiated twoCrepistectorum by (33), whocrossed Crepiswas conducted Gerassimova Selfing a semisterile of F1 translocations. linesthat differed tworeciprocal by for in of was homozygous resulted therecovery a fertile plantthat F2 hybrid with parental lines.Although translocations as a result, semisterile the both and, can individuals be derived by this that recombinant study demonstrated fertile, conclusions can that chromosomally divergent parents, hybridization between of from experiment limited to thesmallnumber generare due be drawn this of barriers amongtheparental ationsanalyzed and theweakness thesterility were in of taxaandtheir derivative. Theselimitations corrected a series hybrid involving Elymus (94), Nicotiana(87), and Gilia comprehensive experiments (40,41). that diverse microspecies morphologically Snyder suggested someofthe (88) in from to grassspeciesElymus glaucusmight factresult assigned theselfing speciesknown to ancestral glaucusand tworelated E. introgression between To in Sitanion jubatumand S. hystrix. testthishypothesis, hybridize nature, of Stebbins generated several hybrids F1 between microspecies E. glaucus (94) the of Although vastmajority F1 florets and either jubatumor S. hystrix. S. of seeds(>99.99%), a smallnumber seedsweregenerated did notproduce by four cases, theF1 seeds werenotusefulbecausetheoffspring Fls. In three of maternal had had either recovered morphology their the parent, undergone F1 a the polyploidization, weresterile.However, singleseed from fourth or from backcross E. had a seed a toward glaucus. Thisplant appeared result to were for The of progeny fertility30% andwas selfed twogenerations. resulting crosseswith seed fertility (88%-100%). Moreover, vigorous had normal and E. almost reproductive isolation; theoriginal glaucusparent indicated complete in from to 3%. 0% of ranged pollenfertility theprogeny thesecrosses of Theseexperiments onlyverified plausibility Snyder's not the hypothesis, of hybrid speciesneed notbe that theyalso indicated theorigin homoploid whentheF1 hybrids reproductive mode,particularly restricted a selfing to are are highly sterile.This is important becausebackcross progeny typically or in moreeasilygenerated morefertile self- sib-crosses early than hybrid and In the speciesused in thesecrosseshave no generations. addition, parental of that chromosomal differences, suggesting it was theassortment apparent in of factors resulted theisolation that than sterility genicrather chromosomal theartificial neospecies. seto unintentional the experiment appears haveinvolved Although Elymus of on for the test lection fertility, first direct oftheeffects selection thegenetic was of hybrids conducted isolation morphological and divergence interspecific interspecific hybrids by Smith& Daly (87) in Nicotiana. Theygenerated N. between large-flowered sanderaeand small-flowered langsdorffii. the N.
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Individual plants F1 withlarge,intermediate, smallflowers and wereused to initiate three self-pollinating hybrid lineages,whichwerethensubjected to selection flower (large, for size and over intermediate, small,respectively) 10 generations. thetenth By generation, linesbred all true both for floral (selected) and vegetative (unselected) morphological characters, statistical and analyses eachother from parental and the revealed the that three lineswere separable from of specieson thebasis of either typeof character. Investigation reproductive from parents barriers revealed also that each selected line was isolated its by meiotic aberration one ormore barriers as crossability, such genetic frequency, and andpollenabortion. Theseresults indicated morphological that divergence in genetic isolation arisefollowing can strong selection self-fertilizing hybrid populations. Themost convincing experimental validation therecombinational of speciationmodelcomesfrom seriesofelegant of a studies 41) involving (40, hybrids Gilia malior x G. modocensis. twospeciesareselfing The annual tetraploids with relatively chromosome a high number = 36). First (2n generation hybrids arehighly sterile, pollen seedfertility2% and0.007%,respectively; with and of in is abnormal meiotic that reduction fertilityduetostrucpairing suggests this tural To ferchromosomal differences between parental the genomes. generate tileandmeiotically the and were normal hybrid lines, most fertile viableplants from natural selection on artificially selected eachgeneration, augmenting thus thesametraits. Although early generation plants wereweakandpartially sterile (hybrid breakdown), vigor fertility and improved rapidly. theF8 andF9, By in had full normal chromosomal and vigor, pairing, full fertility beenrecovered III a three or I hybrid lineages branches. Branch andbranch eachpossessed new II of features whereas branch combination morphological cytogenetic and (40), and reverted largely theG. modocensis to parent both morphologically interms of crossability Gilia (41). As in thecase ofElymus, tworecombinant linthe This isolated from their eageswerestrongly parents (4%-18% pollenfertility). is concordant theoretical with that of isolation expectations thestrength genetic with between and should strongly be correlated derivatives their hybrid parents the barrier between parents themselves strength (39).
TheRole ofGeneInteractions Hybrid in Speciation

The crossing that stablehyexperiments discussed abovedemonstrate fertile, bridlines can arise via crossesbetween isolated bothweaklyand strongly to relative thesenewlinesmaybe morphologically speciesandthat divergent theparents.However, tell abouttheforces thesestudies us little governing the themerger differentiated of or parental speciesgenomes whether results in from are to theseexperimental studies readily extrapolated speciation naet the ture.To address thesequestions, Rieseberg al (79) compared genomic
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annuus lineages (Helianthus synthesized hybrid of composition experimentally (71). Interspecies, anomalus H. hybrid with ofanancient that x H. petiolaris) hybrid genomic and, hybrid fitness indirectly, affect actions amonggenesthat in by parental marker segregation the weredetected analyzing composition lineages. synthesized linI, lineage P-F1-BC lineages weresynthesized: Three hybrid I-BC2-F2-F3; Crosses and eage II, P-FI-F2-BC1-BC2-F3; lineageIII, P-FI-F2-F3-BC1-BC2. a all from givengenpooledpollenfrom plants wereperformed applying by natural that to of eration stigmas thesame individuals-a strategy facilitates the generafor or from final Fifty-six 58 progeny selection increased fertility. H. for surveyed 197 mapped petiolaris tionof each hybrid lineagewerethen composition the wereused to estimate genomic The surveys markers. marker and hybrid of each of the 170 hybrid individually each of thethree progeny lineages cumulatively. of hybrid and synof Comparison the genomiccomposition the ancient all independently,three that generated lineages revealed although thetic hybrid identical genecombinations, converged nearly to hybrid lineages synthesized in to similar thatfound and thisset of gene combinations recognizably was the and between synthetic in composition Concordance genomic H. anomalus. rather than chancelargely governs hyancient that suggests selection hybrids hybrid lineagesweregenerated bridspeciesformation. Because thesynthetic in congruence genomic inthegreenhouse natural conditions, rather under than rather for thanselection selection from fertility appearsto result composition is by to adaptation a xerichabitat.This conclusion supported therapidinin pollenfertility lineages; average creasein fertility observed thethree hybrid Conhybrids. from in Fls to over90% in thefifth generation increased 4% and structure in that genomic the also composition implies gruence genomic within few a fixed of generations speciesmaybe essentially composition hybrid This thereafter. static relatively after initial the event hybridization andremain described above and is studies observation concordant theexperimental with a for speciation. simulation studies (60) that suggest rapidtempo hybrid in distributions theexperimental marker of Analysisof patterns parental hybrid geinto processes governing also hybrids allowedinsights thegenetic of by species differ a minimum ten nomiccomposition.The two parental and plants interchromosomal translocations inversions (Figure2), and hybrid reduced fertility exhibit of rearrangements for heterozygous one ormore these werein thedirecin hybrids (Figure Because all backcrosses thesynthetic 2). individuals tionof H. annuus, selection chromosomally heterozygous against chromosomal the of reduced frequency H. petiolaris appearsto havegreatly that in of portion thegenome-an observation holds fragments therearranged chromosomal and forboththesynthetic ancient lineages. However, hybrid
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375
Analyses associations of amongsegregating parental markers allow detecinteractions tionof specific amongchromosome segments affect that hybrid than fertility, rather thegeneral interactions inferred from frequency the data. is Therationale this for approach that selection favor retention genes will the of The interact of selection that favorably. signature thisepistatic shouldbe deassociations correlations or tectable positive markers by among linked these to interact should detectable be interacting genes.Likewise, genesthat negatively bynegative associations linked these to amongmarkers genes. et To testfortheseinteractions, Rieseberg al (79) analyzed unlinked all infor markers significant and trogressed two-way three-way associations.The werecompelling. ormoresignificant these Ten results from analyses two-way wereobserved each of thethree in associations synthetic hybrid lineages.In themore aspowerful three-way analysis, 29, and 15 significant 21, three-way wereobserved, sociations webs. It is noteworthy generating complex epistatic that eventhough levelswereemployed this in very stringent significance analysis (a < 0.0001), manyof thesame two-and three-way were associations in observed multiple hybrid lineages.Because thehybrid lineagesweregenselection than rather drift must for erated account theseshared independently, markers withepistatic interactions moreoften were associations.Moreover, than markers in found all three that lineages lacking epistasis, suggesting these influence interactions hybrid genomic composition. of The convergence thesynthetic ancient and sunflower hybrid lineages toset warda similar of gene combinations suggests also thathybrid speciation than believed if maybe morerepeatable previously (21). However, thisis the in ask to the case, one might why, contrast thesunflower results, experimenNicotiana(87) and Gilia hybrid tallysynthesized lineages(40,41) diverged in of and Thereare several from each other terms morphology cytogenetics. selection was employed, possiblereasonsforthis. In Nicotiana, diversifying the of in essentially guaranteeing generation divergent lineages.Moreover, both wereinitiated maintained self-pollination and and Nicotiana Gilia,lineages by of single, selected individuals-thus a ensuring majorrolefordrift. conBy sizes of 20 or moreweremaintained Helianthus, in trast, population plants wereoutcrossed, natural and selection was allowed to proceedvia fertility critical is factor that generations backcrossing two of pollenpooling.Another in toward annuuswereemployed thegeneration all three H. of sunsynthetic in flower of hybrid lineages. This appearsto haveresulted theretention that chromosomal subsetofH. petiolaris that in or fragments interacted a neutral manner with H. annuus the toward positive genetic background. Backcrossing to the of H. annuusalso is likely have occurred during formation theancient as in are hybrid species,H. anomalus, backcrosses thisdirection morefertile than other classes(48). andeasilyproduced genotypic
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NATURALHYBRID SPECIES
that The experimental theoretical and studies discussed aboveindicate homoconditions and ploid hybrid speciation a workable is processunder artificial the occurin nature. of maytherefore Nevertheless, actualextent thismodeof is in examspeciation nature unclear.This is notdue to a lack of proposed In literature. fact, there fewmonographs do not are that ples in thetaxonomic to for invoke hybridization account theorigin at leastone or twomorphoof or it logically intermediate mosaictaxa(48,67,90). However, is well known can other thatmorphological forces thanhybridizaintermediacy arisefrom that couldarise tion.Dobzhansky (24), for example, recognized intermediacy evolution.He also notedthat remnants the of by convergent morphological from which twospeciesdifferentiated havetheapmight ancestral population of of (the pearance hybrids-anearlyand explicit recognition plesiomorphy skeptiretention primitive of characteristics). Other authors have expressed cismconcerning use ofquantitative the data hybrids in phenotypic to identify the theabsenceofinformation basisofthecharacters being regarding genetic scored(10,34,47). In many information beenaugmented eviwith studies, morphological has the dencefrom data,and/or secondary chemistry, ecological,and geographic of that the Each ofthese production synthetic hybrids resemble natural hybrids. has but difficult approaches itsstrengths, as with morphological itis often data, whether for to determine characters, ecologicaldistriintermediacy chemical result from And and/or bution, geographic rangeactually hybridity. putative of data biosystematic sets examples hybrid speciesbased on thesetraditional with cannot verified molecular be evidence often (64,74,80,91, 104). a more markers tool identifying taxa Molecular hybrid represent powerful for can As results. with morpho(82), buteventhis approach generate ambiguous a taxadue to markers related of logicalcharacters,taxoncan sharemolecular ancestor thejointretention alleles following of in speciation a polymorphic This has to (symplesiomorphy). phenomenon also been referred as lineage in whendiscussed thecontext genelineagedata(8). As a result, of it sorting the it easiertoreject hypothesis hybrid of than confirm with to is much origin loci markers molecular data sets. The use of multiple (32), linked (25), and the enhances probability distinguishof gene lineagedata (9, 69,74) greatly and if For ingbetween symplesiomorphy hybridization. example, a putative markers potential of and/or linked parents, hybrid speciespossessedmultiple, markers multiple that for at additivity diagnostic parental loci,theprobability thissituation couldbe attributed symplesiomorphyconvergence minito or is becomesan increasingly mized.Likewise, explanation hybridization probable
TheDifficulty Unambiguous of Documentation
377
forshared alleles of identical sequenceas speciesdivergence timesincrease (43). Even ifevidence favor hybridity unambiguous, does notmean in of this is ithad anything do with to speciation. example, For discordant organellar and nuclear phylogenies apparently tohybridization being due are with reported inof creasing frequency buttheevolutionary (83), outcome mostofthese ancient cases ofhybridization to appears be introgression than rather hybrid speciation. The distinction between introgression hybrid and can as speciation be difficult well(101, 104). Incongruence between cytoplasmic- nuclear-based and phylofor genetic that a trees, example, suggest hybridization played roleintheevolution a wildspeciesofcotton, of Gossypium bickii (101). However, is notclear it whether ancient this in hybridization was important itsorigin, G. bickii event as does notappeartohavea biparental nuclear genome typical hybrid of species.
Case Studies
A survey thebotanical of literature identified than putative more 50 of examples homoploid hybrid speciesrepresenting 20 families seed plants.Howover of ever, only17examples havebeenrigorously tested with molecular In markers. my has judgment, homoploid hybrid speciation beenconvincingly documented in eight thesecases (Table 1), whereas theremaining cases, hybrid of in nine speciation disproved 80,91, 104) or themolecular was (78, marker data were with to ambiguous regard hybrid origin 22,64, 101). (1,
HYBRID SPECIES ISOLATED BY POSTMATING BARRIERS The classification of modeofreproductive is hybrid speciesby their isolation somewhat arbitrary as mostprobably have bothpostmating premating and barriers.Premating barriers especially are as to ubiquitous all hybrid speciesappear havediverged their from the ecologically parents.Nonetheless, examples discussedin this section differ do from their parents chromosomal genicsterility or by factors, in whereas those thenext section to appear be isolated primarily tohabitat due differences (Table 1). The first of of application molecular methods thestudy homoploid to hybridspeciation in Stephanomeria was (Compositae) (32). The hybrid species, S. diegensis, its parents, exiguaand S. virgata, self-incompatible and S. are with samediploidchromosome annuals the number = 16). The parental (2n species are widespread largely and allopatric, they co-occurand hybut do in bridize Southern California. First are generation hybrids semisterile (14% due structural differences between pollenviability), apparently tochromosomal theparental species. is native coastalsouthern of Stephanomeria California diegensis anabundant and morphologicallyan "amalgam" itsparents. is of of Analyses 20 isozyme
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of that diegensis S. was a composite thegenesof S. exiguaand loci revealed F1 artificial had onlyone very rareuniqueallele. Furthermore, and S. virgata anditsparents averaged to 2% pollenviabil1% between diegensis S. hybrids the thanthosebetween parental less are ity, thusthey significantly fertile and the proevolution havefacilitated speciation may species.Rapidchromosomal for (below). cess as has beenshown Helianthus have Helianthus speciesofsection Helianthus studies the of annual Molecular to be derived thismode: H. anomalus, via appear three speciesthat identified morphoH. deserticola, H. paradoxus(71,72,74,75,79,81). Although and from all three speciesappearto be derived distinctive allopatric, and logically H. petiolaris) they as combine parental thesametwoparents annuusand (H. DNA units and sharethechloroplast repeat and ribosomal allozymes nuclear the parents, of species. Like their haplotype one or bothparental (cpDNA) number are self-incompatible havea haploidchromosome and three hybrids in of the species,however, terms geographic of 17. Theydiffer from parental is Helianthus to and paradoxus endemic saline distribution habitat preferences. are in H. marshes westTexas,whereas anomalusand H. deserticola brackish United of xericspeciesrestricted theGreatBasin desert thesouthwestern to the throughout central States.By contrast, parental the speciesarewidespread in with annuusfound H. of primarily and western portion theUnitedStates, experiin crossing sandysoils. Artificial mesicsoils and H. petiolaris dry, with parents, ments indicate that three all hybrid speciesare semisterile their barriers (below). due sterility apparently to chromosomal the evolution can facilitate (98) the that To test hypothesis rapidkaryotypic lineageand its between new hybrid a isolation of development reproductive for H. and mapsweregenerated H. annuus, petiolaris, linkage parents, genetic revealed H. comparisons oneoftheir derivatives, anomalus.Geneorder hybrid whereas wereco-linear all 6 species, that ofthe17 linkage among three groups werenotconserved terms geneorder in of 2). 11 (Figure the remaining linkages differed at least 10 by The twoparental species,H. annuusandH. petiolaris, three and inversions, a minimum including rearrangements, structural separate of The species, ofseveninterchromosomal translocations. genome thehybrid 2). (Figure For H. anomalus, extensively relative itsparents to rearranged was 4 of the 11 rearranged H. the arrangement linkages, anomalusshared linkage sevenlinkages, unique ofone parent theother. theremaining or For however, In a of chromosowere arrangements displayed. fact, minimum three linkage to mal breakages, three are fusions, one duplication required achievethe and H. anomalusgenomefrom parents.It is noteworthy all sevennovel that its in rearrangements H. anomalusinvolvelinkagegroupsthatare structurally in that differences may species,suggesting structural divergent theparental Similar chromosomal upon induceadditional rearrangements recombination.
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have mutation ratesfollowing hybridization previincreases chromosomal in in (86). ouslybeenreported grasshoppers remust chromosomal structural differences enhance To reducegeneflow, in productive isolation. Thisdoes appeartobe thecase inH. anomalus, which with pollenstainits are sterile, first generation hybrids with parents partially abilities 1.8%-4.1% (H. annuus)and 2%-58.4% (H. petiolaris)(17,46). of revealed multivalent and fragments Meioticanalyses formations bridges and are for structural differences largely responsible that suggesting chromosomal from inferred evolution hybrid semisterility Thus,therapidkaryotypic (17). through hybrid thesemapping datadoes satisfy genetic modelsforspeciation recombination (98). two Thusfar, oftheexamples hybrid all of speciation haveinvolved parental species cannotbe is reasonwhyadditional species,butthere no particular the involved.An examplecomes from LouisianairiseswhereIris nelsonii (4, from fulva,I. hexagona, I. brevicaulis 6). I. and contains genetic markers plants cannot to very recently, individual as Speciation appears haveoccurred L be unequivocally from hybrid genotypes distinguished either fulvaorcertain zones. However, takenas a whole,the genetic from contemporary hybrid and significantly parental contemporary from make-up I. nelsonii of doesdiffer is in and species stable distinct terms morphology, and of hybrid populations, the ecologicalpreference, karyotype. and Good examplesof hoonly are by barriers aredifficult moploid hybrid speciesthat isolated premating whichappearsto to find.One possibleexampleis Rhodendron intermedium, due and be partially its isolatedfrom parents to soil preferences thebehavior has ofpollinators usingmodern hypothesis notbeentested (51), butKerner's a speciaGrant (38) presented modelforsympatric methods. Morerecently, in of and tion flowering basedonflower constancy pollinators suggested plants in as the that be hybridization might as likely mutation generating newfloral that might represtructures. Straw(96) postulated twospeciesofPenstemon werederived thismanner.However, via senthomoploid hybrid speciesthat this molecular studies notsupport hypothesis do (104). This modeis well-documented Asian pines. Closelyrelated in speciesof and and often fertile vigorare Pinushybridize hybrids frequently, interspecific isolation. due ous. Nonetheless, distinct, apparently to habitat speciesremain several Asian pine speciesare thought be of hybrid to origin (62), Although of is origin theonlyexamplethathas been analyzed rigorously theputative The P P. densatafrom tabulaeformis P yunnanensis. three and specieshave to different with ecologicalrequirements, P. densataendemic highmountain is whereneither its putative of elevations parents found. The geographic
HYBRID SPECIES ISOLATED BY PREMATINGBARRIERS
381
but distribution P densataoverlaps of slightly withbothparents, theparents that themselves allopatric. are Isozymestudies indicate P densatadoes comanalyses cpDNA of binetheallozymes itsputative of parents (100). However, in variation revealed presence three the of cpDNA haplotypes P. densata(99). parents, thethird but couldnot Twowere identical those to found theputative in Wanget al (99) concluded be found extant in Asianpinespecies. As a result, P. via between twoextant that densatamayhavebeen derived hybridization andoneextinct Asianpinespecies. of intotheevolutionary potential A finalstudy thatmayprovide insights the of homoploid hybrid speciation concerns genusPaeonia (85). Additivity in transcribed spacerregion nuof individual nucleotide positions theinternal of clearribosomal genesimplied hybrid a origin a singlespecies,P emodi, as well as that an entire of discovery imis lineageof tenspecies. The latter becauseitsuggests homoploid speciesarenotevolutionary portant that hybrid but and deadends, can found dynamic specioselineages.
THE BIOLOGY OF HOMOPLOID HYBRID SPECIES

include tree, one three perenTheeight confirmed examples hybrid of speciation this is nialherbs, four and annual herbs (Table 1). Although sample toosmallto hybrid speciation, surprising one makevalidgeneralizations abouthomoploid is of The result that haveanoutcrossing all breeding system. presence outbreedto readily ingis unexpected, becausehybrid speciation predicted occurmore is in highly of the proportion inbreeding populations (42,60,98). Likewise, high as annualspeciesofconfirmed is appears hybrid origin unusual hybridization in tobe more frequent perennials. from All oftheproposed confirmed their speciesdiffer parental and hybrid This of as speciesin habitat preference. is expected, course, twospeciescanis the notoccupythesame niche. Whatis unexpected, however, that habitat thanintermeditaxa is often novelor extreme rather occupiedby thehybrid aterelative that theparental the to of species. Examplesinclude highaltitude of habitats thethree of habitat Pinus densata(100) and thexericor marshy Helianthus hybrid species(71). a of confirmed Morphologically, hybrid speciesexhibit largeproportion exor with treme novel characteristics compared their when parents 70,76,78). (34, reAt leastsomeofthismorphological to appears ariseas a direct divergence 33 reveal as of from plant sultofhybridization,studies synthetic genera hybrids in are that over10% ofmorphological characteristics extreme first generation and than30% are extreme latergeneration in hybrids (76). hybrids greater to Thisphenomenon often is referred as transgressive segregation (97), and it in from to than progenies appears be therulerather theexception segregating
382 Table 2
RIESEBERG Isozyme variability confirmed in hybrid species(Hd) andtheir parents (Pt) Percentage Mean no. ofloci ofalleles polymorphica perlocus 23.5 17.6 5.0 5.9 35.3 54.0 41.5 43.6 38.0 61.5 53.8 46.2 36.3 33.6 34.0 1.3 1.2 1.1 1.1 1.5 1.7 1.4 1.6 1.5 2.5 2.8 2.2 2.3 2.6 2.6 Mean heterozygosityb Reference 0.065 0.069 0.022 0.027 0.123 0.167 0.122 0.152 0.134 0.210 0.195 0.169 0.082 0.098 0.109 72 72 72 72 72 6 6 6 6 100 100 100 32 32 32
Taxon Helianthus: annuus (Pt) anomalus (Hd) deserticola (Hd) paradoxus (Hd) petiolaris (Pt) Iris: brevicaulis (Pt) fulva(Pt) hexagona (Pt) nelsonii (Hd) Pinus: densata(Hd) tabulaetormis (Pt) yunnanensis (Pt) Stephanomeria: diegensis (Hd) exigua(Pt) virgata (Pt)
a if aForHelianthus, Iris, and Stephanomeria, locus was considered polymorphic the of frequency themost of common alleledidnotexceed0.99,whereas Pinus,a frequency for a 0.95 was usedtodefine polymorphic locus. whereas bFor Helianthus, andPinus,valuesarefor Iris, meanexpected heterozygosity, for Stephanomeria, valuesrepresent observed meanheterozygosity individual. per
and havespeculated the that morphological interspecific crosses (76). Botanists created hybridization to ecologicalnovelty by might allowhybrid populations ontopreviously spread unoccupied adaptive peaks(3,5,54,93). that taxawouldbe morevariable Earlierworkers predicted hybrid genetithan callyandhavegreater evolutionary potential their parental speciesbecause the this wouldcombine allelesof bothparents 39,93). Although is a they (3, it confirmed reasonable argument,is notsupported datafrom by hybrid species levelsofgenetic Helianthus lower (Table2). Thethree hybrid speciesexhibited as of than diversity either parent measured estimates percentage by polymorof phicloci,meannumber allelesperlocus,andmeanheterozygosity (Table2). whereas more variable than Pinusdensata slightly was genetically either parent, and wereroughly to Stephanomeria diegensis Irisnelsonii equivalent their parlevels entsin terms variability of (Table2). The lower-than-predicted ofdiverof thata smallnumber parental sityin theHelianthus hybrids mayindicate
HYBRIDPLANT SPECIES
383
individuals involved their was in origin, possibly hybrid via founder events as discussed earlier.
CONCLUSIONS AND FUTURE DIRECTIONS

of answers the to Satisfactory understanding anymodeof speciation requires Is evidence for following questions: themodetheoretically possible?Is there is itinnature? How does itoccur?Under what evolutionary conditions itmost likely? How quickly does itoccur?Andhowfrequent it? is Most of thesequestions be answered can for adequately homoploid hybrid As speciation. discussed above,experimental theoretical indicate and data that thismodeis feasible, molecular and marker provide data convincing evidence in for operation nature. its the Likewise, evolutionary processes accompanying this or facilitating mode of speciation well understood. are Important comsuchas thesorting genicand chromosomal of ponents sterility factors, rapid chromosomal and evolution, strong fertility viability selection, ecological and have been verified boththeoretical experimental and studies. divergence by this Manyofthecritical ecological parameters promote modeofspeciation that havealso beenidentified: availability suitable the of hybrid habitat, selective a in for and zone interface, advantage hybrids a hybrid habitat, a long hybrid whichenhances number hybrid the of matings generation. per However, the that observation confirmed hybrid speciesareoutbreeding (Table 1) contradicts theoretical studies that of should increase with indicating rates hybrid speciation the for is selfing (60). Perhaps advantage selfing hybrid of species establishment counterbalanced lower rates natural of by hybridization among selfing lineages. is Less evidence available the and of concerning tempo frequency this mode. However, bothexperimental theoretical pointto a rapidtempoof and data and can be speciation. For example,fertile stablehybrid segregants often after obtained of and studonlya fewgenerations hybridization, simulation is of ies suggest hybrid that zone speciation punctuated: Long periods hybrid linstasisarefollowed therapid by establishment growth thenewhybrid and of in of and eage (62). Congruence genomic composition synthetic ancient hybrid that are to speciesalso suggests hybrid genomes likely be stabilized quickly, with little the of in changethereafter Possibly, tempo speciation natural (79). the chromosomal hybrid speciescouldbe tested analyzing sizes ofparental by sizes in Due decline a predictable fragments. torecombination, fragment should manner overtime(11), perhaps it to the of making feasible estimate number of to a generations hybridization required stabilize hybrid speciesgenome. the in is of Estimating frequency hybrid speciation nature more speculative. in havebeenrigorously documented Onlyeight examples plants (Table 1), and evenfewer animals in that (26), suggesting thismodemaybe rare.However,
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and of of maybe an artifact thedifficulty detecting rigortheselow numbers if species, particularlythehybridization homoploid hybrid ouslydocumenting number hybrid of specieshavebeenproevents ancient.A muchlarger are cases of anstudies continually uncover unexpected posed,and phylogenetic attempts to in lineages(83). Although evolutionary cienthybridization many premature, hybrid speciation probably are estimate frequency homoploid the of in stimulus speciation for may hybridization playa majorroleas thecreative in rates smallor peripheral populations. Hybridization appearto be highest withthesecharacteristics and hybridization be a more may (28), populations the or bottlenecks generating genetic for than plausible mechanism population in founder effect saltational models or reorganization proposed chromosomal ofspeciation (37,71). this substantial progress beenmadein studying mode,much has Although relates theorigin to to A remains be understood. majorgap in ourknowledge by from their parents premating ofhomoploid speciesthat isolated are hybrid in that barriers dataindicate specieshavearisen thismanner, only.Empirical have focusedon thestrict recombiand studies butexperimental theoretical the of sterility national modelthatinvolves sorting genic and chromosomal is it factors. Becausehybrid reticulate rapid, is particularly and speciation both and amenable experimental to manipulation replication.Thus,it shouldbe new speciesisolated feasible to hybrid experimentally synthesize homoploid barriers of studies couldbe only.The design theseexperimental bypremating to mode. informed theoretical studies identify that parameters critical this by genotypes.The issue relatesto the fitness hybrid of Another important modelimpliesthat speciation required thehybrid by ecologicaldivergence of fitness thenewhybrid of exceedthat theparental lineagemust theaverage hybrids habitat.This does notmeanthatearlygeneration speciesin hybrid are morefiton averagethantheir but parents, it does implythe existence in that a advantage hybrid of interspecific combinations convey fitness gene fitnesses couldbe tested comparing lifetime the habitats. This hypothesis by in and habitats.Presumably, of individual genotypes hybrid hybrid parental from several of resulting generations habitat later hybrid segregants generation a The wouldbe mostlikely exhibit fitness to andfertility selection advantage. if of composition wouldbe enhanced thegenomic valueoftheseexperiments the of gene thehybrids known was (79), so that effects particular combinations An wouldbe selection on fitness could be determined. alternative approach to the and of populations that experiments compare responses hybrid parental in habitats selective those (57). approximating expected hybrid regimes the by also remain processes whichnewhyconcerning genetic Questions move to a new adaptive bridspecies arise: 1. How do hybrid populations that is suggest this accomplished genetic mapping experiments peak? Sunflower
385
on selection act directly can thandrift, that and rather by primarily selection it genes. However, is notclear as gene combinations well as all individual is in selection less lineages which is to this whether result generalizable hybrid less from diverlineages hybrid of studies synthetic Detailedmapping intense. 2. this satisfactorily. to gentspeciescrossesmaybe required address question by speciesariseprimarily the in barriers newhybrid reproductive Do postmating or factors via thehighgenicandchrosterility of parental sorting preexisting of populations?This question ratescharacteristic hybrid mosomalmutation of trait the by couldbe addressed comparing locations quantitative loci (QTL) the barriers between parental species to reproductive contributingpostmating If QTL" in its speciesfrom parents. the"sterility isolating hybrid the those with in hythen of taxonarea subset thosefound itsparents, thesorting thehybrid QTL Thepresence unique of sterility inthehybrid wouldbe accepted. pothesis either to as to taxonwouldbe moredifficult interpret, thiscouldbe attributed speciation. following evolution or speciation todivergent evolution during rapid in observed hybrid and novelty fraction the of morphological ecological 3. What evolution following speciaversus divergent by speciesis created hybridization is the issuehere toelucidate dithe the tion?As with previous question, critical in to respect the in speciation case with process, this rect ofhybridizationthe role could this and Although question of origin morphological ecologicalnovelty. of and the be answered comparing morphological ecologicalcharacteristics by haveyettobe made. these and comparisons hybrid species, synthetic natural of phyimportance molecular I the Finally, wantto emphasize continuing species,as these hybrid natural thatidentify document and studies logenetic and about frequency evolutionto studies critical reliable are generalizations the not well,thesestudies onlyprovide ofthismode. Ifdesigned arysignificance but of examplesof the a meansfor"cleansing" literature oft-cited incorrect for also provide efficient an large butthey strategy testing speciation, hybrid of species(71). for of numbers plantand animalgroups theexistence hybrid loci for unlinked andsamplesevthat trees multiple, studies generate Clearly, loci The successful. use ofmultiple is eralpopulations specieswillbe most per to are as gene independent trees required achieve ofparticular importance five will be detected event that (78). Greater 95% confidence a givenreticulation and ancient the resolution will increase chanceofdetecting also phylogenetic lineages. hybrid speciose possibly
ACKNOWLEDGMENTS
Rick Noyes, Jean Pan, Rhonda I thankShanna Carney,Keith Gardner, of and MarkUngerer, Jeannette Whitton, Diana Wolfforcriticism Rieseberg, has research hybrid on themanuscript. author's The speciation beensupported bytheNSF andtheUSDA.
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page at VisittheAnnualReviews home http://www.annurev.org.
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Hybrid Origins of Plant Species Author(s): Loren H. Rieseberg Source: Annual Review of Ecology and Systematics, Vol.

HYBRID ORIGINS OF PLANT SPECIES

WHATIS A HYBRID SPECIES?

HYBRID PLANT SPECIES

HYBRID PLANT SPECIES

THE FREQUENCY OF INTERSPECIFIC HYBRIDIZATION

HYBRID PLANT SPECIES

HYBRID PLANT SPECIES

HYBRID PLANT SPECIES

ESTIMATES OF HYBRID FITNESS

EXPERIMENTAL STUDIES of VerificationtheRecombinational Experimental Model Speciation

HYBRID PLANT SPECIES

TheRole ofGeneInteractions Hybrid in Speciation

HYBRID PLANT SPECIES

annuus anomalus petiolaris annuus anomalus petiolans

shp Fiue2Lnaerltion between Helisynthusze andnncetybis,

HYBRID PLANT SPECIES

TheDifficulty Unambiguous of Documentation

HYBRID PLANT SPECIES

HYBRID PLANT SPECIES

HYBRID PLANT SPECIES

THE BIOLOGY OF HOMOPLOID HYBRID SPECIES

CONCLUSIONS AND FUTURE DIRECTIONS

HYBRID PLANT SPECIES

HYBRID PLANT SPECIES

49. 50. 51. 52. 53.

62. 63. 64.

HYBRID PLANT SPECIES

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