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Book ChapterDOI

Sperm competition in humans

01 Jan 2006-pp 3-31

TL;DR: The classical theory that sperm are small simply because of the difficulties of ensuring that ova do get fertilized may also explain sperm size, and both effects are likely to contribute to the stability of anisogamy.
Abstract: It is suggested that sperm competition (competition between the sperm from two or more males over the fertilization of ova) may account for the fact that sperm are so small and so numerous. In the entire absence of sperm competition, selection may favour an increase in sperm size so that the sperm contributes nutriment to the subsequent viability and success of the zygote. However, an extremely low incidence of sperm competition is adequate to prevent sperm size increasing. Vertebrate sperm should remain at minimal size provided that double matings (one female mated by two males) occur more often than about 4 times the ratio of sperm size:ovum size. The classical theory that sperm are small simply because of the difficulties of ensuring that ova do get fertilized may also explain sperm size, and both effects (sperm competition and ensuring fertilization) are likely to contribute to the stability of anisogamy. Large numbers of sperm can be produced because sperm are tiny and the optimal allocation of reproductive reserves to ejaculates is not trivially small even when double matings are rather rare. It is suggested that of its total mating effort, a male vertebrate should spend a fraction on sperm that is roughly equivalent to a quarter of the probability of double mating.
Topics: Sperm (69%), Sperm competition (68%)

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Adaptation to Sperm
Competition in Humans
Todd K. Shackelford and Aaron T. Goetz
Florida Atlantic University
ABSTRACT—With the recognition, afforded by recent evo-
lutionary science, that female infidelity was a recurrent
feature of modern humans’ evolutionary history has come
the devel opment of a unique area in the study of human
mating: sperm competition. A form of male–male postcopul-
atory competition, sperm competition occurs when the
sperm of two or more males concurrently occupy the re-
productive tract of a female and compete to fertilize her ova.
Males must compete for mates, but if two or more males have
copulated with a female within a sufficiently short period of
time, sperm will compete for fertilizations. Psychological,
behavioral, physiological, and anatomical evidence indi-
cates that men have evolved solutions to combat the adap-
tive problem of sperm competition, but research has only
just begun to uncover these adaptations.
KEYWORDS—sperm competition; anti-cuckoldry; sexual
conflict; female infidelity; evolutionary psychology
Male flour beetles sometimes fertilize females with a rival male’s
sperm. This ‘‘fertilization by proxy’’ occurs when the mating
male’s aedeagus (reproductive organ) translocates the sperm of
another male into the female’s reproductive tract (Haubruge,
Arnaud, Mignon, & Gage, 1999). The sperm of a male that a
female has copulated with can adhere to a subsequent male’s
aedeagus because these insects’ genitalia have chitinous spines
designed to facilitate removal of rival male sperm prior to dep-
osition of self-sperm into a female’s reproductive tract. This
phenomenon was predicted and observed by researchers who
study sperm competition. Although not yet document ed empir-
ically, humans also may experience fertilization by proxy
(Gallup & Burch, 2004). More generally, a rapidly growing lit-
erature indicates that sperm competition has been an important
selection pressure during human evolution.
Sperm competition is intrasexual (male–male) competition
that occurs after the initiation of copulation. Whereas Darwin
and others identified precopulatory adaptations associated with
intrasexual competition (e.g., horns on beetles, status seeking
in men), researchers studying sperm competition aim to identify
postcopulatory adaptations. Thus, an alternative way of thinking
about sexual selection is that there is not only competition
between males for mates, but competition between males for
fertilizations.
Sperm competition is the inevitable consequence of males
competing for fertilizations. If females mate in a way that con-
currently places sperm from two or more males in their repro-
ductive tracts, this generates selection pressures on males. If
these select ion pressures are recurrent throughout a species’
evolutionary history, males will evolve tactics to aid their sperm
in outcompeting rivals’ sperm for fertilizations. These tactics
may take the form of anatomical, physiological, and psycho-
logical adaptations. Although revolutionary for its time, the first
definition of sperm competition, ‘‘the competition within a single
female between the sperm of two or more males for the fertili-
zation of the ova’’ (Parker, 1970, p. 527), does not capture the full
spectrum of male anatomy, physiology, psychology, and behavior
associated with sperm competition .
SPERM COMPETITION AS AN ADAPTIVE PROBLEM IN
HUMANS
For species that practice social monogamy—the mating system
in which males and females form long-term pair bonds but also
pursue extra-pair copulations (i.e., ‘‘affairs’’)—it is the extra-
pair copulations by females that creates the primary context for
sperm competition. A male whose female partner engages in an
extra-pair copulation is at risk of cuckoldry—the unwitting in-
vestment of resources into genetically unrelated offspring—and
its associated costs, which include loss of the time, effort, and
resources the male spent attracting his partner and the misdir-
ection of his current and future resources to a rivals offspring.
Consequently, in species with paternal investment in offspring,
selection often favors the evolution of adaptations that decrease
Address correspondence to Todd K. Shackelford, Florida Atlantic
University, Department of Psychology, 2912 College Avenue, Davie,
FL 33314; e-mail: tshackel@fau.edu.
CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE
Volume 16—Number 1 47Copyright r 2007 Association for Psychological Science

the likelihood of being cuckolded. Anti-cuckoldry tactics fall
into three categories: preventative tactics, designed to prevent
female infidelity; sperm competition tactics, designed to minim-
ize conception risk in the event of female infidelity; and differ-
ential paternal investment, designed to allocate paternal
investment prudently in the event that female infidelity may
have resulted in conception.
The extent to which sperm compet ition occurred in ancestral
human populations would have depended largely on rates of
female sexual infidelity and cuckoldry. Current est imates of
worldwide cuckoldry rates range from 1.7% to 29.8% (Ander-
son, 2006). Although current estimates of cuckoldry rates pro-
vide only a proxy of the occurrence of cuckoldry throughout
human evolutionary history, even the most conservative esti-
mates of these rates would have generated sufficient selection
pressures on males to avoid the costs of cuckoldry. Moreover, the
ubiquity and power of male sexual jealousy provides evidence of
an evolutionary history of female infidelity and thus perha ps also
of sperm competition. Male sexual jealousy can evolve only if
female sexual infidelity was a recurrent feature of human evo-
lutionary history, and female infidelity increases the likelihood
that sperm from two or more men occupied concurrently the
reproductive tract of a particular woman. This suggests that
sexual selection, in the form of sperm competition, has been an
important selection pressure during recent human evolution. If
this is the case, then specific adaptations to sperm competition
may have evolved.
ADAPTATIONS TO SPERM COMPETITION IN HUMANS
In this section, we discuss adaptations men may have evolved in
response to an evolutionary history of sperm competition. We
limit our discussion of these adaptations to testis size, ejaculate
adjustment, semen displacement, sexual arousal, and forced in-
pair copulation, as these adaptations have been investigated
more rigorously than others.
Testis Size
Across a range of animal species, males have relatively larger
testes in species with more intense sperm competition. Because
larger testes produce more sperm, a male with larger testes can
better compete by inseminating a female with more sperm.
Among the great apes, testes size varies predictably with the risk
of sperm competition. In gorillas, female promiscuity and sperm
competition are rare, and the gorilla’s testes are relatively small,
making up just 0.03% of their body weight. Chimpanz ees, in
contrast, are highly promiscuous and, accordi ngly, males have
relatively large testes, making up 0.30% of their body weight.
The size of human testes falls between these two extremes at
0.08% of body weight, suggesting intermediate levels of female
promiscuity and sperm competition in our evolutionary past
(Shackelford & Goetz, 2006).
Ejaculate Adjustm ent
The number of sperm recruited into a given ejaculate is not
constant. Although the physiology is not well understood, there
is evidence that sperm number can be adjusted even moments
before ejaculation (reviewed in Shackelford, Pound, & Goetz,
2005). A key hypothesis derived from sperm competition theory
is that males will adjust the number of sperm they inseminate
into a femal e as a function of the risk that their sperm will en-
counter competition from the sperm of other males. Baker and
Bellis (1993) documented a negati ve relationship between the
proportion of time a couple has spent together since their last
copulation and the number of sperm ejaculated at the couple’s
next copulation. As the proportion of time a couple spends to-
gether since their last copulation decreases, there is a predict-
able increase in the probability that the man’s partner has been
inseminated by anot her male. Additional analyses documented
that the proportion of time a couple spent together since their last
copulation negatively predicts sperm number ejaculated at the
couple’s next copulation, but not at the man’s next masturbation
(Baker & Bellis, 1993). Inseminating into a female more sperm
following a separation may function to outnumber or ‘‘flush out’’
sperm from rival men that may be present in the reproductive
tract of the woman.
Inspired by Baker and Bellis’s (1993) demonstration of male
physiological adaptations to sperm competition, Shackelford
et al. (2002) documented that human male psychology may in-
clude psychological adaptations to decrease the likelihood that a
rival man’s sperm will fertilize a partners ovum. For example,
men who spent a greater proportion of time apart from their
partners since the couples’ last copulation—and, therefore, face
a higher risk of sperm competition—report that their partners
are more sexually attractive, have more interest in copulating
with their partners, and believe that their partners are more
interested in copulating with them, relative to men spent a lesser
proportion of time apart from their partners. These effects were
independent of relationship satisfaction, total time since last
copulation, and total time spent apart, which rules out several
alternative explanations (although other plausible alternative
mechanisms remain to be evaluated). These perceptual changes
may motivate men to copulate as soon as possible with their
partners, thereby entering their sperm into competition with any
rival sperm that may be present in their partners’ reproductive
tracts.
Semen Displacement
Features of the peni s may have evolved in response to the se-
lective pressures of sperm competition. The penis of the dam-
selfly is equipped with spines that can remove up to 99% of the
sperm stored in a female, and the penis of the tree cricket is
designed structurally to remove rival sperm prior to insemin-
ation of the male’s own ejaculate. Spines, ridges, and knobs on
the penis of some waterfowl are positioned in a way to displace
48
Volume 16—Number 1
Sperm Competition

rival sperm, and these protuberances are larger in species for
which the intensit y of sperm competition is greater.
The human penis does not have barbs and spines for removing
rival sperm, but recent evidence suggests that the human penis
may have evolved to function, in part, as a semen-displacement
device. Using artificial genitals and simulated semen, Gallup
et al. (2003) tested the hypothesis that the human penis is de-
signed to displace semen deposited by other men in the repro-
ductive tract of a woman. The results indicated that artificial
phalluses with a glans and coronal ridge that approximated a
human penis displaced more simulated semen than did a phallus
that did not have such features. When the penis is inserted into
the vagina, the frenulum of the coronal ridge makes semen
displacement possible by allowing semen to flow back under
the penis alongside the frenulum and collect on the anterior of
the shaft behind the coronal ridge. Displacement of simulated
semen occurred when a phallus was inserted at least 75% of its
length into the artificial vagina.
That the penis must reach an adequate depth before semen is
displaced suggests that displacing rival semen may require
specific copulat ory behaviors. Following allegations of female
infidelity or separation from their partners (conte xts in which the
likelihood of rival semen being present is relatively greater),
both men and women report that men thrusted the penis more
deeply and more quickly into the vagina at the couple’s next
copulation (Gallup et al., 2003), behaviors likely to increase
semen displacement. In an independent study, Goetz et al.
(2005) investigated men’s copulatory behav iors when under a
high risk of sperm competition. Men mated to women who placed
them at high risk of sperm competition were more likely to use
specific copulatory behaviors arguably designed to displace
rival semen (e.g., more frequent thrusts, deeper thrusts) than
were men mated to women who did not place them at high risk of
sperm competition.
Sexual Arousal
Men’s sexual fantasies often involve sex with multipl e, an-
onymous partners—behavior that would have had fitness payoffs
in ancestral environments. It has been suggested, however, that
although men might desire and seek sexual variety and the ab-
sence of competition with other men, cues of sperm competition
risk also might be sexually arousing. Because sexual arousal
increases the rate of sperm transport in the vas deferens, Pound
(2002) argued that ancestral males might have benefited from
being aroused to cues of sperm competition. When faced with
cues of sperm competition, sexual arousal would have resulted in
an increase in sperm transport upon ejaculation, thus enabling
men to compete more effectively in such contexts.
Pound hypothesized that men, therefore, will be more aroused
by sexually explicit image s incorporating cues of sperm com-
petition than by comparable material in which such cues are
absent. Content analyses of sexually explicit images on Internet
sites and of commercial ‘‘adult’’ video releases revealed that
depictions of sexual activity involving a woman and multiple
men are more prevalent than those involving a man and multiple
women, indicating that the former category may be preferred by
men. Additionally, an online survey of self-reported preferences
and an online preference study that unobtrusively assessed
image selection yielded corroborative results. Pound argued that
the most parsimonious explanation for these results is that male
sexual arousal in response to visual cues of sperm competition
reflects the functioning of psychological mechanisms that would
have motivated adaptive patterns of copulatory behavior in an-
cestral males exposed to evidence of female promiscuity.
Pound’s hypothesis recently has been supported by experi-
mental evidence that men viewing images depicting cues to
sperm competition produce more competitive ejaculates than
men viewing comparable images in which cues to sperm com-
petition are absent (Kilgallon & Simmons, 2005). Kilgallon and
Simmons documented that men produce a higher percentage of
motile sperm in their ejaculates after viewing sexually explicit
images of two men and one woman (sperm competition images)
than after viewing sexually explicit images of three women. More
generally, these results support the hypothesis that men adjust
their ejaculates in accordance with sperm competition theory.
Forced In-Pair Copulation
Noting that instances of forced in-pair copulation (i.e., partner
rape) followed extra-pair copulations in waterfowl and anecdotal
reports that forced in-pair copulation in humans often followed
accusations of female infidelity, Thornhill and Thornhill (1992)
hypothesized that sexual coercion in response to cues of a
partner’s sexual infidelity might function in humans to introduce
a man’s sperm into his partner’s reproductive tract at a time when
there is a high risk of extra-pair paternity. Goetz and Shackelford
(2006a) found empirical support for this hypothesis. In two
studies, Goetz and Shackelford found that men’s sexual coercion
in the context of an intimate relationship was related positively
to his partner’s infidelities. According to men’s self-reports and
women’s partner-reports, men who use more sexua l coercion in
their relationships are mated to women who have been or are
likely to be unfaithful. The hypothesis that sexual coercion and
forced in-pair copulation may be a sperm competition tactic has
been supported directly and indirectly in at least half a dozen
studies (reviewed in Goetz & Shackelford, 2006b).
CONCLUSION AND FUTURE DIRECTIONS
Sperm competition was first identified as a form of postcopula-
tory competition between males by Geoff Parker in the 1970s.
Since then, evolutionary biologists and behavioral ecologists
have described many anatomical, physiological, and behavioral
adaptations to sperm competition in many nonhuman species.
The question as to whether sper m competition has been an
Volume 16—Number 1 49
Todd K. Shackelford and Aaron T. Goetz

important selection pressure during human evolution remains
somewhat controversial, and further research is needed to es-
tablish the extent to which this might be the case. As outlined in
this article, however, there is mounting evidence that aspects of
men’s sexual psychology and behav ior, such as their attraction to
and sexual interest in their partners, their copulatory behaviors,
and sources of sexual arousal, may reflect adaptations to sperm
competition.
Although we focused on men’s adaptations to sperm compe-
tition, women are not passive sperm receptacles. An important
avenue for future research is to identify adaptations not only in
men but also in women. Sexual conflict between males and fe-
males produces a coevolutionary arms race between the sexes, in
which an advantage gained by one sex selects for counterad-
aptations in the other sex. Thus, men’s adaptations to sperm
competition are likely to be met by counteradaptations in women
(e.g., mechanisms that increase retention of sperm inseminated
by men with ‘‘good genes’’; see Shackelford et al., 2005), and the
study of such mechanisms is an important direction for future
research.
Recommended Reading
Platek, S.M., & Shackelford, T.K. (Eds.). (2006). Female infidelity and
paternal uncertainty. New York: Cambridge University Press.
Shackelford, T.K., & Goetz, A.T. (2006). (See References)
Shackelford, T.K., & Pound, N. (Eds.). (2006). Sperm competition in
humans. New York: Springer.
Shackelford, T.K., Pound, N., & Goetz, A.T. (2005). (See References)
Acknowledgments—The authors contributed equally to this
article.
REFERENCES
Anderson, K.G. (2006). How well does paternity confidence match
actual paternity? Evidence from worldwide nonpaternity rates.
Current Anthropology, 47, 513–520.
Baker, R.R., & Bellis, M.A. (1993). Human sperm competition:
Ejaculate adjustment by males and the function of masturbation.
Animal Behaviour, 46, 861–885.
Gallup, G.G., & Burch, R.L. (2004). Semen displacement as a sperm
competition strategy in humans. Evolutionary Psychology, 4,
12–23.
Gallup, G.G., Burch, R.L., Zappieri, M.L., Parvez, R.A., Stockwell,
M.L., & Davis, J.A. (2003). The human penis as a semen dis-
placement device. Evolution and Human Behavior, 24, 277–289.
Goetz, A.T., & Shackelford, T.K. (2006a). Sexual coercion and forced in-
pair copulation as sperm competition tactics in humans. Human
Nature, 17, 265–282.
Goetz, A.T., & Shackelford, T.K. (2006b). Sexual coercion in intimate
relationships: A comparative analysis of the effects of women’s in-
fidelity and men’s dominance and control . Manuscript submitted
for publication.
Goetz, A.T., Shackelford, T.K., Weekes-Shackelford, V.A., Euler, H.A.,
Hoier, S., Schmitt, D.P., & LaMunyon, C.W. (2005). Mate retention,
semen displacement, and human sperm competition: A prelimi-
nary investigation of tactics to prevent and correct female infi-
delity. Personality and Individual Differences, 38, 749–763.
Haubruge, E., Arnaud, L., Mignon, J., & Gage, M.J.G. (1999). Fertili-
zation by proxy: Rival sperm removal and translocation in a beetle.
Proceedings of the Royal Society of London B, 266, 1183–1187.
Kilgallon, S.J., & Simmons, L.W. (2005). Image content influences
men’s semen quality. Biology Letters, 1, 253–255.
Parker, G.A. (1970). Sperm competition and its evolutionary conse-
quences in the insects. Biological Reviews, 45, 525–567.
Pound, N. (2002). Male interest in visual cues of sperm competition
risk. Evolution and Human Behavior, 23, 443–466.
Shackelford, T.K., & Goetz, A.T. (2006). Comparative evolutionary
psychology of sperm competition. Journal of Comparative Psy-
chology, 120, 139–146.
Shackelford, T.K., LeBlanc, G.J., Weekes-Shackelford, V.A., Bleske-
Rechek, A.L., Euler, H.A., & Hoier, S. (2002). Psychological
adaptation to human sperm competition. Evolution and Human
Behavior, 23, 123–138.
Shackelford, T.K., Pound, N., & Goetz, A.T. (2005). Psychological and
physiological adaptations to sperm competition in humans. Review
of General Psychology, 9, 228–248.
Thornhill, R., & Thornhill, N.W. (1992). The evolutionary psychology of
men’s coercive sexuality. Behavioral and Brain Sciences, 15, 363–
421.
50 Volume 16—Number 1
Sperm Competition
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TL;DR: Psychological, behavioral, physiological, and anatomical evidence indicates that men have evolved solutions to combat the adaptive problem of sperm competition, but research has only just begun to uncover these adaptations.
Abstract: With the recognition, afforded by recent evo- lutionary science, that female infidelity was a recurrent feature of modern humans' evolutionary history has come the development of a unique area in the study of human mating:spermcompetition.Aformofmale-malepostcopul- atory competition, sperm competition occurs when the sperm of two or more males concurrently occupy the re- productivetractofafemaleandcompetetofertilizeherova. Malesmustcompeteformates,butiftwoormoremaleshave copulated with a femalewithina sufficiently short periodof time, sperm will compete for fertilizations. Psychological, behavioral, physiological, and anatomical evidence indi- cates that men have evolved solutions to combat the adap- tive problem of sperm competition, but research has only just begun to uncover these adaptations. KEYWORDS—sperm competition; anti-cuckoldry; sexual conflict; female infidelity; evolutionary psychology

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