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Glossary
Delayed fertilization
Due to delayed ovulation: copulation and insemination occur long before
ovulation. The opposite of this trait is induced ovulation, where the release
of one or more mature eggs occurs soon after mating.
Due to sperm storage: copulation and insemination are followed by a period
over which sperm are maintained in the females reproductive tract for an
extended period, after which the egg is fertilized by these stored sperm.
Delayed implantation: fertilization occurs shortly after mating [5]. Cell division
and development occur to the blastocyst stage (200300 cells) but the
conceptus remains in the uterine lumen for an extended period of time instead
of immediately implanting into the uterine lining.
Female sperm storage (FSS): extended maintenance of viable sperm within the
females reproductive tract. FSS is a general phenomenon that encompasses
the terms delayed fertilization and delayed ovulation. FSS results primarily
from selection on females but can also be influenced by selection on males.
Male sperm storage (MSS): extended maintenance of mature sperm in the
epididymis before mating.
Sperm longevity: the reproductive life expectancy of sperm independent of any
female processes (i.e., without female aid but under the same general
conditions).
Sperm storage: extended maintenance of viable sperm within the reproductive
tract (male or female). Implicit and often untested is that the sperm must be
capable of fertilization at the end of storage.
Sperm viability: refers to the capacity of sperm to successfully fertilize eggs. A
viability of 50% or greater is considered to be a demonstration of fertility based
on the human infertility literature [39].
Trends in Ecology & Evolution, May 2015, Vol. 30, No. 5
261
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availability [1,5,6]. Similarly, males may benefit from manipulating sperm storage inside the female by biasing
paternity on their favor or by increasing their overall
paternity from any one mating (e.g., Drosophila; Box 1).
However, the benefits to males from storing sperm before
copulation have been discussed less, although they can be
just as important because they can pre-adapt sperm to
survive longer inside the female and sperm are unlikely to
be used immediately after spermatogenesis. Males can
benefit from storing sperm before mating if separating
sperm production from sperm delivery is advantageous.
Sperm-storing males can have sperm ready to use during
the reproductive season earlier than other males [58] or, if
males spread the costs of reproduction between gamete
production and obtaining a mate, this strategy is likely to
be adaptive [79].
At present, we lack a framework that unites the selective forces responsible for purported sperm-storage traits
(3)
(4)
(5)
(6)
(7)
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1.
Copulaon
2.
Ejaculaon
Sperm from
3.
vagina to uterus (bursa)
Movement
Uterus changes shape,
expands
4.
Storage
(FSS)
5.
Sperm
release &
ovulaon
Sperm to storage
organs: receptacle and
spermatheca
Sperm released
from storage, eggs
ovulated*
6.
Sperm used to
Ferlizaon ferlize eggs
Sperm mass
(sperm +
ejaculate)
Seminal
receptacle
Spermatatheca
SSs
Sperm move to
storage structures
where they remain
mole.
Sperm movement
from stores.
Sperm in receptacle
more likely to ferlize
(uorescent studies).
Parovaria
Figure I. A schematic representation of the key steps and molecules involved in sperm storage in Drosophila melanogaster.
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Box 2. Sperm storage is widespread and nearly ubiquitous in internal fertilizers, as seen in this phylogeny
Colors indicate the number of species known to have sperm storage
in each branch. Fertilization mode is indicated as I (internal) or E
(external) or a combination, with the most common type listed first.
Ferlizaon
Key:
Duraon Locaon
Most FSS
Many FSS
Some FSS
None FSS
Suspected FSS
Alligators
Birds
Turtles
Lizards
Snakes
Bats
Other placental mammals
Marsupials
Monotremes
Amphibians
Lungsh
Coelacanths
Bony sh
Sharks and rays
Urochordates
Hagsh and lamprey
Hemichordates
Echinoderms
Cnidarians
Ctenophorans
Arthropods
Nemotodes
Flatworms
Lophorates
Annelids
Mollusks
Sponges
I
I
I
I
I
I
I
I
I
I/E
E
I
I/E
I/E
E
E
E
E
E
E/I
I
I
I
E/I
I
E/I
E
7
7-117
90-1,460
14-540
90-2,555
16-300
0.5-30
0.5-16
unk.
120-900
90-240
30-730
14-4,000
5
55
180-365
70-1,460
-
Oviduct
SSTs in uterovaginal juncon
Albumin glands in oviduct
SSTs, sacs, crypts in oviduct, infundibulum, vagina, uterovaginal junct.
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Anatomy
Physiology
Behavior
12 criteria
SSI = (sum of supported criteria N criteria
examined)/total criteria
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Box 4. The strength of selection on FSS can be visualized in various taxa using our suggested SSI
Note that values in parentheses have partial support (and thus are
weighed as 0.5 rather than 1 in SSI calculations). Here we also
Aributes
Variable
Annelid
Shark
Life
history
Mammal:
Marsupial
Amphibian
illustrate sperm-storage anatomy in various taxa (anatomical illustrations by T.J.O.) (Figure I).
Mammal:
Human
Mammal:
Bat
Reple
Bird
Mollusk:
Snail
Insect:
Fruit y
Insect:
Honey bee
MSS*
Physiology
Structures (organs)
Region
Mulple types of
storage sites
Sperm in organized
arrangement
Female localized
immune suppression
Sperm receive
nourishment
Sperm have specialized
biochemistry
Ovulaon only at end of
SS
Behavior
SSI
Sum of evidence
N lines of evidence
Index (SSI)
( )
( )
( )
( )
( )
( )
( )
4
5
1.7
5
5
2.1
4.5
6
2.3
6
7
3.5
5
9
3.8
5.5
9
4.1
6.5
8
4.3
8
9
6.0
9
9
6.8
8.5
11
7.8
12
12
12
Anatomy
Figure I. An illustration of how the SSI can be applied to taxa where some criteria for sperm storage are known. General anatomical features associated with sperm
storage in each group are also depicted.
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Table 1. Example species illustrating the variety of methods used to assign the presence of sperm storagea
Invertebrates
Arthropoda
Crabs (various over
Decapoda
110 species) including
(Brachyura)
Pseudocarcinus gigas,
Chionoectes bairdi
Spiders (generalized)
Arachnida
Insecta
Gastropoda
Duration (days)
Location
Evidence
Refs
14 years
including some
with trans-molt
retention
365
Thelycum, spermatheca,
seminal receptacle
[18]
[8,36]
140
Spermatheca
14 or longer
Spermatheca
3550 or longer
Seminal conceptacles
(sperm-storage
receptacles and transport
ducts in oviducts and
elsewhere modified from
immune cells)
Spermatheca and seminal
receptacles
[72]
[31]
[33,54]
14
Panamanian leaf-cutting
ant (Atta colombica)
>3650
Spermatheca
Odonata (dragonflies
various species)
Days to >2
weeks
Spermatheca
At least length
of reproductive
season
Until
spawning
Achatinidae, Helicidae
>365
Subdivided spermatheca
or spermathecal tubule
Earthworm (Hormogaster
elisae)
820
Spermathecae
[48]
Nematode
(Caenorhabditis elegans)
[33]
Uterine glands
[40]
138
Uterotubal junction
Unknown
Unknown
Unknown
Uterine cornua
[10]
0.523
[33,56]
[43]
[55]
[20]
[35]
[73]
Annelida
Chromadorea
Mammals
Theria
[74]
[9]
[1,28]
267
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Table 1 (Continued )
Duration (days)
0.6
Location
Lower isthmus of oviduct
0.9
30
Uterus
Quoll (Dasyurus
viverrinus)
Opossum (Didelphis
virginiana)
Dunnart (Sminthopsis
macroura)
Fat-tailed dunnart
(Sminthopsis
crassicaudata)
Evidence
Refs
[1]
[1]
Uterine glands
[21]
6
2.0
Uterus
Uterus
[1]
[1]
14
[1,53]
0.5
[1,53]
2.5
[1,53]
2.5
Brown antechinus
(Antechinus stuarti)
16
Echidna (Tachyglossus
sp.)
Implied
[1,67]
Marsupials
[1,53]
Unknown
[51]
300
Histology
[15]
300
Ovary micropocket
[75]
365
Oviduct tubules
[66]
390
Histology
[34]
1316
SST in uterovaginal
junction
Histology; controlled-mating
experiments, some demonstrating
motility
[1]
11117
8
1316
SST
SST
SST
120
Uterus or vagina
90
Vaginal furrows
[1]
Monotremes
Fish
Osteichthyes
Chondrichthyes
Blue shark (Prionaca
glauca)
Gummy shark (Mustelus
antarcticus)
[12]
Amphibia
Tailed frog (Ascaphus
truei)
Aves
Passeriformes
Galliformes
Columbiformes
Anseriformes
Reptilia (Squamata)
Snakes
Neotropical rattlesnake
(Crotalus durissus
terrificus)
268
[1,38,51]
[1]
[1]
[11]
[1,31]
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Table 1 (Continued )
Duration (days)
Location
Evidence
Refs
Unknown
[13]
Fringe-fingered lizard
(Acanthodactylus
scutellatus)
Green anole (Anolis
carolinensis)
Tropical house gecko
(Hemidactylus mabouia)
120
210
Sperm receptacles
[1,30]
Unknown
[44]
1095
Albumin-secreting glands
in oviducts
Albumin-secreting glands
in oviducts
SST, isthmus
(infundibulum
oviduct to uterus)
[76]
Lizards
[1,13]
Turtles
730
120
[76]
[52]
Sperm storage has been described in a many taxa using various criteria. Even within the same taxon, the criteria used to assign FSS differ between studies. Data include
duration, location (if known), and other supportive evidence.
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of sophistication in the morphology of sperm-storage structures can reflect the strength of selection and costs and
constraints in evolution. For example, sperm-storage
tubules in birds have a single opening and sperm are lined
up in the order in which they enter the tubule. As a result,
the last sperm to enter is the first to exit, leading to lastsperm precedence in birds [51]. In spiders, females place
sperm from separate matings into different storage organs
[49]. This might reflect a different degree of precopulatory
choice that selects for more refined sperm-storage organs
if females have less control over mating.
In species lacking specialized sperm-storage organs,
selection on females can still favor sperm storage, and
such storage might occur in structures of the female reproductive tract that originally evolved for other functions.
For example, the uterine glands of dogs [20], albuminsecreting glands in turtles [52], and the oviductal glands
of sharks [15] have been found to contain sperm and have
been suggested as storage sites. However, it is unknown
whether sperm simply arrives in these sites by chance
and are easily trapped because of their architecture and
location [28], so the mere presence of sperm within these
structures is not sufficient evidence of FSS. The best
support that these are sperm-storage organs would be
information on whether sperm from these structures are
used to fertilize eggs. In the absence of such data, examining multiple individuals would reveal at least whether
sperm reliably end up in the same location. Other anatomical lines of evidence could include examination of epithelial differences (ultrastructure) in regions of putative
storage. For example, the presence of glandular tissue
could be investigated for secretion of sperm-nourishing
materials (criterion number 4).
Further evidence that females store sperm in the absence of specialized storage organs could derive from the
examination of ontogenetic changes of the putative spermstoring regions. If sperm-storing features are apparent
only when a female reaches sexual maturity, this is supportive that such features play a role in FSS. However,
anatomical or physiological changes that occur in the
reproductive tract after mating could result from selection
on both males and females and coevolutionary processes.
Changes induced by copulation have been observed in
the epithelial folds of the brushtail possum (Trichosurus
vulpecula) [50], secretory cells in the soft-shelled turtle
(Lissemys punctata) [52], the grey short-tailed opossum
(Monodelphis domestica) [29], and the cervix of some mammals [40]. If the mechanism by which these structures
become modified to store sperm is derived from chemical
or mechanical changes that occur during copulation, males
have the potential to manipulate females to preferentially
store their sperm.
Wherever they are located, putative sperm-storage sites
must be conducive to fertilization either because of proximity to ovulated eggs or because sperm can be moved from
these stores to areas where unfertilized oocytes occur. The
fat-tailed dunnart (Sminthopsis crassicaudata) moves
sperm from crypts closer to the oviduct around ovulation
[53]. In cephalopods (e.g., Architeuthis) sperm are moved
from under the skin of their arms to fertilization sites
[14]. Another extreme example of sperm movement is seen
270
in the traumatically inseminated bed bug (Cimex lectularius), which has evolved specialized structures to direct
sperm to newly derived (from mesoderm versus ectoderm
as in other insects) storage organs [54]. Other females
might move sperm to particular areas [33]; for example,
to sites where males cannot remove them (Odonata [55]).
If sperm consistently position themselves or are positioned
by the female in putative storage sites, this could be taken
as support of FSS and the role of these structures in sperm
storage.
Strength of selection on sperm storage and weighing
the evidence for FSS
Sperm storage is widespread and diverse in species with
internal fertilization and we need a more refined way to use
data to understand patterns of sperm-storage evolution,
including the action of the various mechanisms of selection
that act on adaptations to store sperm. One way to achieve
this understanding is to use the criteria outlined above to
determine the relative support for different mechanisms of
selection acting on various species. We have developed a first
approximation in the form of a simple quantitative index
(Box 3) where individual criteria are weighed differently to
examine the evolution of FSS. This could also be done for
MSS, to examine selection on males once their sperm are
inside the female, and to study coevolutionary processes
after further refinement of the criteria we present. Further,
this approach will allow us to examine the phylogenetic
patterns of the various criteria for sperm storage and their
correlation with the ecologies of animals with differing
levels of support for sperm storage (Box 2). Our proposed
SSI might have utility for comparing taxa (such as those
outlined in Table 1) and could reveal surprising and previously unappreciated patterns in sperm storage.
Concluding remarks and future directions
We were prompted to write this article due to frustration
with the lack of clarity in studies of sperm storage, which
seem to assume that any sperm storage is equivalent to
FSS. We hope to have shown that this is not necessarily
the case and that different mechanisms of selection on
males and females can act on sperm storage. Further, we
also call attention to the fact that multiple selective mechanisms can affect sperm storage and that these sources
of selection should be distinguished in future studies. We
outline (Box 5) a few ideas for future research into sperm
storage. We view this synthesis as a call for greater
attention to this issue rather than as a definitive set of
conclusions and hope other biologists will use our ideas as
a starting point for studies of the prevalence and evolution
of sperm storage mediated by selection on males and
females.
Acknowledgments
The authors thank Jeff Podos, Thomas Eiting, Casey Gilman, Duncan
Irschick, Norman Johnson, Diane Kelly, the OEB graduate program, Paul
Craze, and two anonymous reviewers for useful comments on early drafts
of the manuscript. Dr Mariana Wolfner helped us to clarify the molecular
pathways in Drosophila shown in Box 1. The authors also thank Marlene
Zuk for insightful discussions. T.J.O. was supported by a National Science
Foundation Postdoctoral Research Fellowship in Biology under Grant
No DBI-297 1202871.
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