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International Journal of Primatology, Vol. 23, No. 4, August 2002 (°
Sexual Selection and Mate Choice
Andreas Paul1
Received May 22, 2001; accepted August 15, 2001
After a long period of dormancy, Darwin’s theory of sexual selection in general, and mate choice in particular, now represents one of the most active
fields in evolutionary research. After a brief overview of the history of ideas
and a short introduction into the main mechanisms of sexual selection, I discuss some recent theoretical developments and empirical findings in the study
of mate choice and review the various current models of mate choice, which
can be grossly divided into adaptive models and nonadaptive models. I also
examine whether available primate evidence supports various hypotheses concerning mate choice. Although primatologists were long aware that nonhuman
primates have preferences for certain mating partners, until recently the functions and evolutionary consequences of their preferences remained obscure.
Now there is growing evidence that mate choice decisions provide primates
with important direct or indirect benefits. For example, several observations
are consistent with the hypothesis that by direct or indirect mate choice female
primates lower the risk of infanticide or enhance the chance of producing viable offspring. Nevertheless, there are also significant holes in our knowledge.
How the male mandrill, one of Darwin’s famous examples, got his brightly
colored face, is still unknown.
KEY WORDS: sexual selection; sex roles; mate choice; polyandrous mating; nonhuman
primates.
That the males of all mammals eagerly pursue the females is notorious to every one. . . .
The female, on the other hand, is less eager than the male.
Darwin (1871)
1 Universität
Göttingen, Institut für Zoologie und Anthropologie, Berlinerstr. 28, D-37073
Göttingen, Germany; e-mail: paul [email protected].
877
C 2002 Plenum Publishing Corporation
0164-0291/02/0800-0877/0 °
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One of the numerous examples Darwin referred to in The Descent of
Man, and Selection in Relation to Sex (1871) was the mandrill (Mandrillus
sphinx), one of the most sexually dimorphic primate species. “No other member in the whole class of mammals,” he noted, “is coloured in so extraordinary
a manner as the adult male mandrill” (Darwin, 1998, p. 558). In Darwin’s
view, the evolution of highly exaggerated, flamboyant, ornamental and apparently useless traits such as the male mandrill’s face or the male peacock’s
tail, which abound throughout the animal kingdom, were difficult to explain
by natural selection. His solution was the theory of sexual selection, which
he defined as “the advantage which certain individuals have over others of
the same sex and species solely in respect of reproduction” (p. 216). This
advantage could arise by two ‘kinds of sexual struggle’: “In the one it is
between individuals of the same sex, generally the males, in order to drive
away or kill their rivals, the females remaining passive; whilst in the other,
the struggle is likewise between the individuals of the same sex, in order to
excite or charm those of the opposite sex, generally the females, which no
longer remain passive, but select the more agreeable partners” (p. 638). The
male mandrill, he suggested, “appears to have acquired his deeply-furrowed
and gaudily-coloured face from having been thus rendered attractive to the
female” (p. 560).
While Darwin’s first mechanism of sexual selection—male-male competition over access to females—‘the law of battle’—was readily accepted by
his contemporaries and scientific peers, virtually none of them was convinced
by the seemingly strange view of females as active, strategic decision-makers
based on a more than dubious aesthetic sense. But Darwin’s most ingenious
idea was not only in strong opposition to the Victorian and post-Victorian
Zeitgeist. Because of its seemingly useless and often even deleterious effects
for the species as a whole it also contradicted what most biologists for a fairly
long time took for granted: that natural selection always acts for the good of
the species (Mayr, 1972). This neatly led to Julian Huxley’s (1942) view of
sexual selection (or interspecific selection, in general) as a ‘biological evil.’
As a consequence, and in spite of the work of a few pioneers such as Fisher
(1915, 1930), Bateman (1948), and Maynard Smith (1956), it took a full century until the ‘crown jewel of evolutionary theory’ (Hrdy, 1999) was taken
serious by evolutionary biologists (Cronin, 1991; Miller, 2000; Trivers, 1972;
West-Eberhardt, 1979, Williams, 1966, Zahavi, 1975).
Since the 1970s, the theory of sexual selection and mate choice has
experienced a fulminant revival, with major new theoretical insights and
empirical findings (Andersson, 1994; Birkhead, 2000; Birkhead and Møller,
1998; Eberhard, 1996). Perhaps most significantly, research in the area has
led to a considerable change of views about the relative roles of males
and females in the evolutionary process. In particular, the stereotype of
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aggressive, ardent males competing over access to essentially passive, coy
females is increasingly being shown to be inappropriate (Birkhead, 2000).
Although rarely mentioned in the nonprimatological literature (Andersson,
1994), primatological research has undoubtedly contributed to this progress
(Hrdy, 1981, 1986; Hrdy and Williams, 1983; Smuts, 1992). However, partly
because female choice is difficult to measure in natural settings, primatologists have focused more often on the effects of male competition, leading
to the somewhat paradoxical situation that we apparently “know less about
female choice in non-human primates than we do about female choice in
the Tungara frog, the guppy fish, or the African widowbird” (Miller, 2000,
p. 184). For this reason, and because excellent recent reviews on related
topics such as mating systems, sperm competition and sexual dimorphism
in bodily and canine size are available elsewhere (Dixson, 1998; Gomendio
et al., 1998; Harcourt, 1996; Kappeler, 1997; Kappeler and van Schaik, this
issue; Plavcan, 2000), I will largely restrict my review to questions related to
mate choice. Moreover, I do not thoroughly review the literature on mate
choice in primates, but instead concentrate on some of the theoretically most
important questions and empirical findings.
MECHANISMS OF SEXUAL SELECTION
Darwin’s two mechanisms of sexual selection, male–male competition
by sexual combat and female choice, are still among the major concepts of
modern sexual selection theory (Andersson and Iwasa, 1996), though the
two kinds of sexual struggle are neither as easily distinguished, as Darwin
believed (Wiley and Poston, 1996) nor the only mechanisms of sexual selection. Recognition that sexual selection can continue after insemination via
sperm competition (Parker, 1970) and ‘cryptic’ female choice, i.e. selection
of certain gametes within the female reproductive tract (Eberhard, 1996),
were 2 major advances in the study of sexual selection. Moreover, only after
researchers had recognized that selection does not always act for the good
of a species (Williams, 1966), they also recognized that the relation between
the sexes is far from harmonious and that males often use coercive tactics in
order to maximize their reproductive success (Smuts, 1992).
Finally, during the past few decades it has become increasingly clear
that neither competition over access to mates nor mate choice is restricted
to one sex (Cunningham and Birkhead, 1998; Johnstone et al., 1996) and both
components of sexual selection can take several forms (Table I). For example, competition over access to mates does not necessarily consist of fights
between males over females. Although fertilizable eggs are principally a nonshareable resource, in cases wherein spatiotemporal distribution of females
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Table I. Mechanisms of sexual selection
Mechanism
Mate competition
Endurance rivalry
Scramble competition
Contest competition
Reproductive suppression
Sperm competition
Alternative mating tactics
Mate choice
Precopulatory choice
Postcopulatory choice
Postfertilization choice
Male counterstrategies
Sexual coercion
Explanation
Remaining reproductively active for long periods
Finding a mate before rivals do
Excluding rivals by display or physical combat
Suppression of rivals’ gonadal function by
socioendocrinological mechanisms
Competition between ≥2 rival sperm for the fertilization
of ova
Inconspicuous mating behavior by sneaky copulations,
female mimicry, or searching for females away from
physically superior males
A behavioral pattern that restricts the probability of fertile
matings with particular partners
A mechanism that enables a female to select among the
sperm of different males in her reproductive tract
Selection between the zygotes, embryos or young
produced by different males via differential abortion or
differential investment in offspring
The use of force or threat of force to increase the
probability that a member of the opposite sex will
engage in fertile matings at some cost to the recipient
prevents males from monopolizing fertilizations, competition can also be of
the scramble type, in which favored males are able to locate and to fertilize
females before their rivals do. In this case, sexual selection favors attributes
such as speed and well-developed sensory organs, but not necessarily large
size or strong weapons (Andersson, 1994; Andersson and Iwasa, 1996).
The complex relationships between Darwin’s two mechanisms of sexual
selection have recently been clarified by Wiley and Poston (1996). According to them, competition for mates consists of behaviors that tend to expand
an individual’s set of potential mates. In contrast, mate choice includes all
behavior by an individual “that restricts membership in its set of potential
mates” and therefore is characterized by a decrease, rather than an increase,
in the set of potential mates (Wiley and Poston, 1996, p. 1373). However,
mate choice is not necessarily restricted to active discrimination, or direct
mate choice, among possible mates. Any other behavior or signal that restricts the chances of mating with particular individuals of the opposite sex
can be called indirect mate choice. Examples of indirect mate choice are
synchronization of sexual cycles or advertisement of female reproductive
state by sexual swellings, pheromones or mating calls, which attract and thus
stimulate interference competition among males. The distinction between
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direct and indirect mate choice has two important implications. First, by indirect mate choice, females set the conditions for male competition, making
the two mechanisms of sexual selection inseparable. Secondly, while direct
female choice often results in exaggerated, even bizarre, male morphology,
indirect female choice might produce bizarre morphology in females, such
as elaborate perineal swellings of some female primates.
SEX ROLES AND SEXUAL SELECTION
Perhaps because Darwin belonged to a species in which males seem to
be more concerned than females with the attractiveness of potential sexual
partners (Jones, 1995), he was well aware of the fact that mate choice is not
necessarily restricted to females. Nevertheless, until recently, it was generally
assumed that only one sex, usually the female, engages in active choice (but
see Parker, 1983). The theoretical framework for the different roles of the
sexes was laid out by Trivers (1972). Building on experiments by Bateman
(1948), he argued that the key variable controlling the operation of sexual
selection is the relative parental investment of the sexes in their young:
investment in an offspring that reduces the parent’s ability to invest in other
offspring. In his classic experiments with fruit flies, Bateman had shown that
variance in male reproductive success (RS) exceeded variance in female
RS, and male, but usually not female, RS increased with the number of
mates. He argued that sexual selection should be stronger on males than
on females. Trivers (1972) expanded this framework by arguing that when
one sex invests more in their young than the other does, members of the
more investing sex will become a limiting resource for the members of the
less investing sex. Competition over mating opportunities with members
of the more investing sex would thus be an unavoidable consequence of
differential parental investment. Since in fruit flies, as well as in most other
species, fathers invest much less in their progeny than mothers do, males
are expected to compete over access to fertilizable females. An empirical
measure of this sex bias in reproduction is the operational sex ratio (OSR),
i.e., the ratio of fertilizable females available to sexually active males at any
given time (Emlen and Oring, 1977). Trivers (1972) also argued that the
relative parental investment of the sexes affects the criteria of mate choice:
When parental investment of one sex strongly exceeds that of the other,
members of the former sex are expected to be selective in choice of a mate.
Trivers’ (1972) approach clearly represented a major advance in the
study of sexual selection; however, it does not explain the variation in male
and female sexual selection among species with exclusive male parental care
(Andersson, 1994; Andersson and Iwasa, 1996). For example, in three-spined
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sticklebacks (Gasterosteus aculeatus), males are more brightly colored than
females, suggesting that sexual selection is stronger in males, despite the fact
that males alone care for the brood. Therefore, and because parental investment is notoriously difficult to quantify (Clutton-Brock, 1991), CluttonBrock and Vincent (1991) proposed that differences in the potential reproductive rates of males and females predict variation in the strength of
sexual selection much better than the relative parental investment of the
sexes does. Although stickleback males are limited in the number of eggs
for which they can care (Kraak and Bakker, 1998), their potential reproductive rate is higher than that of females since the latter prefer to spawn
with males whose nests already contain eggs from other females (Ridley and
Rechten, 1981), and males can inseminate and guard up to 6 clutches at a
time (Andersson, 1994). Hence, despite exclusive male care, the operational
sex ratio is biased towards males, making sexual selection stronger among
them. Nevertheless, in most cases, and most obviously in mammals, the potential reproductive rate of a sex will depend on the parental investment it
makes (Andersson, 1994), and whether the operational sex ratio, the maximum reproductive rate of the sexes or some other aspect most closely reflects
the strength of sexual selection is still a matter of debate (Andersson and
Iwasa, 1996).
Recent research also suggests that mutual mate choice may be relatively common (Cunningham and Birkhead, 1998; Johnstone et al., 1996;
Kraak and Bakker, 1998; Sandvik et al., 2000). Male choice is expected to
occur when females differ in quality, when males seek long-term partners or
when they are otherwise constrained in their ability to mate with multiple
females, and/or when they allocate resources to females or their offspring
(Cunningham and Birkhead, 1998). Accordingly, mutual mate choice might
be most common in monogamous species where both sexes have similar
parental roles (Andersson, 1994), but there is also some evidence for mutual mate choice in promiscuous species (Kraak and Bakker, 1998).
Finally, Darwin’s (1871) view of males eagerly pursuing choosy, but
otherwise essentially coy and passive females, which was later both empirically and theoretically substantiated and perpetuated by Bateman (1948) and
Trivers (1972), received considerable criticism (Hrdy, 1986), sometimes even
to the point that there may be something wrong with the theory (Gibbons,
1992; Small, 1993, p. 114). In fact, there is growing evidence that females
of many species, including many mammals (van Noordwijk and van Schaik,
2000) copulate with multiple males (Birkhead, 2000). Moreover, in many
cases, females are not just accepting copulations by eager males but actively
approach and solicit copulations by several males. From the perspective
of the Bateman-Trivers scenario this is indeed surprising, since females, in
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contrast to males, generally cannot increase the number of offspring they
produce by mating with more than one sexual partner; sex role-reversed
species are the exception that proves the rule. Moreover, since mating entails costs (Daly, 1978), mating with multiple males also entails additional
costs which may shorten a female’s life-span: time and energy devoted
to courtship and copulation, increased risk of predation and/or harassment
by conspecifics while mating, risk of disease from parasitic transmission,
negative effects of some seminal fluid products transferred by males during
mating, and, in species wherein mothers rely on the help of their mates for
successful reproduction, reduced male care due to lower certainty of paternity (Eberhard, 1996; Gomendio et al., 1998; Keller and Reeve, 1995).
Yet, several studies have shown that despite the costs, females copulating with multiple males are reproductively more successful than females
with only one partner (Birkhead, 2000). Indeed, although Bateman (1948,
p. 362) explicitly noted that in fruit flies “the males show direct proportionality between number of mates and fertility,” while “the females, provided
that they have been mated at least once, show absolutely no effect of number of mates,” his experiments with food-limited individuals revealed exactly this effect: not only male but also female RS increased by multiple
mating (Arnold and Duvall, 1994). While such an effect is expected in socalled sex role-reversed species (Andersson, 1994; Trivers, 1972), it is not
always well understood why female RS at least occasionally increases with
the number of copulation partners in nonreversed species. In some cases, as
in Bateman’s fruit flies, multiple mating might simply serve to insure fertilization. Bateman speculated that food-limited males might produce fewer
sperm and females needed to recopulate to replenish their sperm supply
to maintain high egg fertility. However, although sperm depletion has been
found in a variety of animals (Dewsbury, 1982), polyandrous mating is not
a decision sine qua non in this situation: if males differ in their fertilization
ability, females might discriminate against males with reduced sperm supply (Andersson, 1994). Apart from the fertilization insurance hypothesis, a
number of alternative hypotheses have been proposed to explain polyandrous matings (Gomendio et al., 1998; Halliday and Arnold, 1987; Keller
and Reeve, 1995; van Noordwijk and van Schaik, 2000; Zeh and Zeh, 1996).
THEORIES OF MATE CHOICE
While Darwin was not able to provide a satisfactory explanation for
why female (or male) choosiness evolved, his followers suggested possible solutions, several of which eventually received substantial theoretical
and empirical support. Theories of mate choice can be grossly divided into
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Table II. Theories of mate choice
1 Direct benefits
2 Indirect benefits
2.1 Fisherian runaway process
2.2 Genetic indicator (good
genes) mechanisms
2.2.1 Handicap models
2.2.2 Host-parasite
coevolution
2.3 Heterozygosity hypothesis
2.4 Genetic compatibility
hypothesis
3 Nonadaptive hypotheses
3.1 Sensory bias hypothesis
3.2 Chase away hypothesis
Choosy sex gets resources
Choosy sex gets only genes
Traits are favored in spite of a cost of reduced
viability because individuals with large
ornaments are more attractive to members
of the opposite sex and sire more attractive
offspring
Traits are favored because they indicate high
heritable quality
Traits are favored because they are costly, and
therefore honest indicators of high heritable
quality
Traits are favored because they indicate high
parasitic resistance
Females choose genetically dissimilar partners to
increase the degree of heterozygosity
in their offspring
Females mate with multiple partners to minimize
the risk of being inseminated by genetically
incompatible sperm
Choosy sex gets nothing
Traits are favored because they exploit an already
existing bias in the species’ sensory system
Exaggerated traits are favored to overcome
female resistance against suboptimal mating
due to a preexisting sensory bias
models assuming either direct (material) or indirect (genetic) fitness benefits
for the choosy sex—adaptive models (Table II)—and models assuming no
fitness benefits for the choosy sex at all: nonadaptive models (Table II).
Adaptive Models I: Direct Benefits
Direct phenotypic benefits of mate preferences such as increased likelihood of successful fertilization, or trading sex for resources such as food,
protection or parental care, are widespread in the animal kingdom (Knight,
1991), easy to understand, and may also provide a possible explanation for
the incidence of multiple mating by females. Moreover, if direct benefits
are present, they are likely to have a much greater effect on female fitness
than any indirect benefits (Price et al., 1993). But often, females appear
to gain nothing more from a copulation than the male’s sperm. Although
even here some direct benefits such as disease avoidance could be involved
(Kirkpatrick and Ryan, 1991), it is generally assumed that in such cases, mate
choice may result from a genetic association between male attractiveness and
offspring fitness.
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Adaptive Models II: Indirect (Genetic) Benefits
The two most widely known models of mate choice that assume a
genetic association between male attractiveness and offspring fitness are
Fisher’s (1930) ‘runaway process’ and several versions of the ‘good-genes’
model (Fisher, 1915; Hamilton and Zuk, 1982; Trivers, 1972; Wilkinson et al.,
1998; Williams, 1966; Zahavi, 1975). According to Fisher’s runaway model,
females gain indirect genetic benefits by choosing attractive males, not because they are genetically superior in any way, but because females with
a strong preference for attractive males will have attractive sons and, ultimately, more grand-offspring than females mating with less attractive males.
The critical feature of Fisher’s process is a genetic correlation between female
preference and the preferred male ornament, which occurs in sticklebacks,
for example (Bakker, 1993). Once established in a population, the female
mating preference can become self-reinforcing, leading to the exaggeration
of the ornament beyond the point at which it is advantageous. In contrast,
good-genes models suggest that male secondary sex traits are not arbitrary
features, but have evolved to reflect a male’s inherent quality such as his
resistance against pathogens. Thus, by choosing an attractive male, a female
acquires viable genes for her offspring.
While genetic models have shown that the Fisherian self-reinforcing
runaway selection is theoretically possible (Andersson, 1994), until recently
there was little empirical evidence that this process occurs in nature
(Andersson, 1994; Ryan and Kirkpatrick, 1991). However, research on fruit
flies (Etges, 1996), lekking sandflies (Jones et al., 1998), field crickets (Wedell
and Tregenza, 1999) and guppies (Brooks, 2000) provide substantial support
for Fisher’s theory. In the case of lekking sandflies there is no evidence that
females mating with attractive males increased their fitness directly or that
they benefited from enhanced offspring survival. Instead, Jones et al. (1998)
found that the mating success of sons increased with the attractiveness of
their fathers. Similarly, in guppies the only detectable benefit to females that
mate with attractive males was that they sired attractive sons, even though
the offspring of attractive males suffered from substantial fitness costs due
to a negative genetic correlation between male attractiveness and survival
(Brooks, 2000). The good-genes model also received empirical support across
a large range of taxa (Møller and Alatalo, 1999). Although the magnitude of
viability effects appears to be relatively small in most cases, they may have
considerable fitness consequences on an evolutionary time-scale.
Both the Fisherian runaway model and the good-genes models assert
that there is a genetic advantage for females that choose the best available
male and that he is the best for every female. But there are at least two reasons
why this may not always be the case. First, there is considerable inter- and
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intraindividual variation in choosiness (Jennions and Petrie, 1997; Waynforth
and Dunbar, 1995; Widemo and Sæther, 1999), suggesting that mating preferences are neither species-specific nor uniform. Secondly, there are good
reasons to assume that what is best for one female may not be best for another
(Brown, 1997). Partly, this idea dates back to Trivers (1972), who suggested
that females might obtain good genes for their offspring by “choosing a male
whose genes complement her own, producing an ‘optimal’ diversity in the
offspring.” For example, there is abundant evidence that heterozygosity is
generally beneficial to individuals (Brown, 1997), and that inbreeding avoidance mechanisms evolved to reduce the probability of homozygous alleles
with lethal or deleterious effects (Pusey and Wolf, 1996). Moreover, like sexuality itself, in fluctuating environments mate choice based on heterozygosity
and genetic diversity may be an adaptation that favors the production of superior competitors (Bischof, 1985; Brown, 1997). Observations that in some
species females prefer to mate with males carrying dissimilar alleles of the
major histocompatibility (MHC) complex (Penn and Potts, 1999) provide an
example, though it is not yet clear whether the main function of MHC-based
mate preferences is inbreeding avoidance, enhanced immunocompetence,
or that it provides hosts a moving target against rapidly evolving parasites
(Penn and Potts, 1999). Brown (1997) also suggested that the frequently
observed preference for mates with a low degree of fluctuating asymmetry
(Møller and Thornhill, 1998) has its genetic basis not so much in better genes
as in greater heterozygosity, though in this case all females should prefer the
same best male.
A similar idea to the heterozygosity hypothesis is the genetic incompatibility hypothesis (Zeh and Zeh, 1996, 1997), which suggests that females
have evolved postcopulatory choice mechanisms that prevent them from
being fertilized by genetically incompatible sperm. Like the heterozygosity hypothesis, but in contrast to other hypotheses based on inherent male
genetic quality, the genetic incompatibility hypothesis asserts that sperm
quality is a relative characteristic that depends, at least in part, on the genotype of the female herself. As indicated by high rates of early spontaneous
abortion in many plants, animals and humans (Penn and Potts, 1999; Zeh
and Zeh, 1996), genetic incompatibility of gametes which arises partly from
intragenomic conflicts appears to be widespread, rendering the assumption
that the nuclear and cytoplasmatic genomes of any female can be combined
with the nuclear genome of any male increasingly unrealistic (Zeh and Zeh,
1996).
Three important implications arise from these data: First, precopulatory mate choice based on male phenotype appears to provide little scope
for females to match male genotype against their own (Zeh and Zeh, 1997).
Odor-based discrimination of male MHC-types is an exception (Penn and
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Potts, 1999; Wedekind and Füri, 1997). Consequently, females may only be
able to minimize the risk and/or cost of fertilization by genetically incompatible sperm by mating with more than one male (Zeh and Zeh, 1996, 1997).
Second, polyandrous mating is likely to be most beneficial for viviparous
taxa such as mammals in which both fertilization and embryonic development occur within the female, because it provides females with a mechanism
to reduce the cost of fertilization with incompatible sperm, which is not available to females laying eggs (Zeh and Zeh, 1997). Third, polyandrous mating
might be most effective in species producing mixed-paternity litters, because
the females have the opportunity to allocate resources directly from genetically defective to viable embryos (Zeh and Zeh, 1997). While Zeh and Zeh
(1997) asserted that there is extensive circumstantial evidence supporting
their hypothesis, the genetic incompatibility hypothesis is, of course, not
the only one explaining polyandrous mating. Alternative hypotheses assert
that females may acquire good genes from extrapair fertilizations with genetically superior males or several direct benefits such as additional male
parental care.
Nonadaptive Models
Nonadaptive models of mate choice suggest that traits might be favored
as incidental byproducts of viability selection because they happen to fit an
already existing bias in the species’ sensory system. In cases of ‘sensory
exploitation’ (Ryan, 1990) the signal in effect creates a sensory trap to manipulate behavior in the signaler’s own favor (West-Eberhard, 1984). The
idea was developed further by Holland and Rice (1998), who suggested that
the evolution of exaggerated male display traits might be based on cyclic
antagonistic, rather than reinforcing, coevolution between the sexes. Their
chase-away model of sexual selection assumes that preexisting sensory bias
of females selects males to evolve an initial, rudimentary display trait that
enhances their attractiveness to them. If the overly attractive males induce
females to mate in a suboptimal manner, females are expected to evolve
counter-adaptations, i.e., resistance against the male display trait, rather than
a preference for it. This, in turn, would select males to evolve even more extreme display traits to overcome the increased receiver threshold, and cyclic
antagonistic coevolution ensues. Thus, in contrast to other established models of sexual selection, the chase-away model predicts that female attraction
to male display traits reduces her net fitness, and consequently, that females
evolve diminished attraction to male display traits. While several observations appear to be consistent with the model (Holland and Rice, 1998), not
all cases of sensory exploitation may be nonadaptive for the choosy sex. For
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example, the ‘eye-spots’ on a peacock’s “tail” may catch the female’s attention due to a preexisting sensory bias (Ridley, 1981), but in this case females
mating with males with more elaborate trains appear to gain indirect benefits
in terms of good genes (Petrie, 1994). Alternatively, and perhaps more likely
the sensory biases might be a starting point for a Fisherian runaway process.
In conclusion, there are several models to explain mate preferences and
none of them appears to be operating at the exclusion of others, though their
relative importance may vary (Holland and Rice, 1998).
PRIMATE STUDIES
While there is abundant evidence for male and female mate preferences
and mate choice in humans (Buss, 1994) and other animals (Andersson,
1994), the situation for nonhuman primates appears to be much less clear.
For example, while Smuts (1987) was convinced that female choice represents a major force in the evolution of primate societies, Cords (1987) noted
that female choice may be important, but that at present only anecdotal evidence exists for it. Two thorough reviewers of the field reached even more
skeptical conclusions. Keddy-Hector (1992) concluded that “the evidence
for female mate choice in most species of non-human primates is modest at
best,” and Small (1989) found that her most significant finding was “the lack
of any conclusive evidence for female choice in primates.” There are several
reasons for this uncertainty. First, in contrast to many other, fast-breeding
species, experiments designed to test predictions derived from sexual selection theory are virtually absent for any nonhuman primate. Second, until
now, almost no study incorporated genetic paternity analyses with systematic behavioral observations on sexual interactions and mate choice in natural settings (but see Constable et al., 2001; Fietz et al., 2000; Kuester et al.,
1994; Pereira and Weiss, 1991; Soltis et al., 2001). Third, because male and
female reproductive interests are rarely congruent, theories of sexual conflict and sexual dialectics (Gowaty, 1997) predict highly variable, dynamic,
and often antagonistic sexual tactics, making it notoriously difficult to assess
their relative importance (Andersson and Iwasa, 1996). For example, even
if females have preferences for certain males (and most studies assume that
this is the case), they may rarely be able to exercise free female choice, i.e.,
choice unconstrained by female-female competition, male-male contests, reproductive suppression, male choice, or male coercion (Gowaty, 1997). In
species characterized by female dominance over males, or codominance of
the sexes, females may be better able to exercise free female choice (Pereira
and Weiss, 1991), but even here competition between males may result in
that only certain high-ranking males are available for females (Kraus et al.,
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1999). Thus, perhaps more often than is usually appreciated, females may
only respond to offers they could not refuse (Hrdy, 1999; Fedigan, 1982).
Is There Evidence for Mate Choice in Nonhuman Primates?
Despite their skeptical conclusions, previous reviewers of mate choice in
nonhuman primates revealed that females of many species not only actively
solicit sexual interactions with males but also often display clear preferences
for certain males and reject solicitations of others (Dixson, 1998; KeddyHector, 1992; Manson, 1995a; Small, 1989; Smuts, 1987), suggesting that
female choice is a potentially powerful selective force among nonhuman
primates (Manson, 1992). In fact, there is considerable evidence for both
direct and indirect mate choice in nonhuman primates. A preference for
dominant males is one of the most often reported findings (Small, 1989),
though this preference is by no means universal. For example, based on
long-term paternity data in a captive group of rhesus macaques, Smith (1994)
speculated that females actually do not prefer top-ranking males, but instead
younger ones that ultimately achieve top rank. Systematic analyses of female
proximity maintenance behavior showed that among rhesus and Japanese
macaques, male attractiveness is not correlated with their dominance rank
(Manson, 1992; Soltis et al., 1997a,b, 2001). The females prefered males of
various dominance ranks, but were monopolized by dominant males, which
prevented them from mating with mid- and low-ranking males (Manson,
1992, 1994a; Soltis et al., 2001). Nevertheless, a female preference for males
signaling their physical superiority by morphological or behavioral traits or
both appears to be widespread (Boinski, 1987: squirrel monkeys; Soltis et al.,
1999: Japanese macaques; Steenbeek, 2000: Thomas’s langurs; van Schaik
and van Hooff, 1996: orangutans; Watts, 1990: gorillas).
Female mate preferences may also be based on former affiliative relationships in nonsexual contexts with certain males—friendships—an idea
that was first developed in depth by Smuts (1985) for savanna baboons. But
although friendships appear to be widespread among primates, recent work
on baboons and macaques indicates that they are typically established as a
result of prior sexual activity (Bercovitch, 1991; Palombit et al., 1997) and
that they rarely have a positive impact on future matings (Bercovitch, 1991;
Huffman, 1991; Manson, 1994b). Quite in contrast to the friendship hypothesis, several studies showed that females often have a strong preference
for unfamiliar or novel males (Bercovitch, 1997; Small, 1989). Although
Manson’s (1995b) systematic study of mate choice in rhesus monkeys led
him to suggest that females may be seldom able to exercise a preference
for novel males, several recent paternity studies provide evidence that such
preferences at least sometimes affects reproductive outcomes (Berard et al.,
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1994; Fietz et al., 2000; Gagneux et al., 1997; Launhardt et al., 2001; but see
Constable et al., 2001).
As expected by various models of mate choice, there is also considerable evidence for individual variation in mate preference (Huffman, 1991:
Japanese macaques; Strier, 1997: muriquis). Although the basis for such preferences remains unclear in many cases, at least one clear pattern emerges:
a strong aversion to mate with close childhood associates, which is a proximate mechanism to avoid incestuous mating (Westermarck, 1891). Incest
avoidance among matrilineally-related individuals occurs in all major taxa
of primates (Dixson, 1998; Pusey, 1990; Wolf, 1995), and paternity studies
confirmed that the aversion strongly lowers the probability that such individuals will produce offspring together (Kuester et al., 1994; Smith, 1995). However, the lower-than-expected frequencies of mating between relatives that
are resident in the same group are restricted to maternal relatives (Kuester
et al., 1994) and to paternal relatives from the same age cohort (Alberts,
1999; Paul and Kuester, unpubl. results), suggesting that the Westermarck
effect is responsible for the avoidance of incestuous matings. Whether other
kin recognition mechanisms such as MHC-related odor cues also influence
mate choice decisions among nonhuman primates, as appears to be the case
in humans (Wedekind and Füri, 1997), remains to be investigated. The lack
of incest avoidance among paternal relatives born at intervals greater than
one or two years suggests that such cues, if present, are probably of minor
importance.
One of the most consistent findings is that female primates mate with
multiple, and often, with as many males as possible, rather than seeking
copulations with one, or a few best males (Bercovitch, 1995; Strier, 1997;
Taub, 1980). However, this does not necessarily mean that fertile matings
are random, and mechanisms enabling females to choose males indirectly
also appear to enable them to choose both certain males and other males,
though at different stages of their reproductive cycles.
Finally, there is good evidence that not only men but also nonhuman
male primates are choosy. Although systematic, quantitative analyses
of male mate choice decisions are rare, the typical pattern found in nonhuman primates is that males prefer older experienced females, high-ranking
females (Anderson, 1986; Keddy-Hector, 1992), or ones with large perineal
swellings (Domb and Pagel, 2001).
Is There Evidence for Direct or Indirect Benefits of Mate
Choice in Primates?
While there is broad agreement that female and male primates have
preferences for certain sexual partners and that they avoid others, the
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evolutionary consequences of such choices appear to be much less clear.
Why, for example, should female nonhuman primates mate with dominant
males? Of course, it is possible that good genes are involved, since although
male dominance hierarchies are often quite unstable and the actual position
of a male may not advertise his genetic quality, it seems unlikely that all
males will be able to achieve top positions during their lives. Conversely,
at least among primates, achieving and maintaining high rank appears to
depend more on help from others than on the genetic design of the individual (Harcourt and Stewart, 1986). Moreover, genetic paternity analyses
revealed that among captive rhesus macaques both the rank and the RS of
natal males were strongly correlated with mother’s rank, but not with their
father’s rank (Smith and Smith, 1988).
Strong evidence that females get direct benefits from mating with dominant males appears to be limited, too. Brown capuchins provide an intriguing, but isolated, example (Janson, 1984, 1986, 1994). In populations where
they depend on small food trees during the dry season when fruit is scarce,
all females consistently prefer to mate exclusively with the dominant male.
Since the dominant male only tolerates juveniles at food trees that he could
have sired, females gain substantial direct benefits of having mated with him.
Notably, in populations of brown capuchins (and white-fronted capuchins)
wherein males are unable to control resources that limit female reproduction, females do not consistently prefer top-ranking males. Undoubtedly,
male control of resources that limit female reproduction is an important aspect of female mating decision in human societies (Hrdy, 1997), but both the
human and the capuchin cases nicely illustrate that preferences for powerful,
resource-controlling males are conditional. Trading sex for resources such
as meat has also been observed in chimpanzees and bonobos, but whether
male chimpanzees enhance their attractiveness as mating partners by foodsharing or other social services is controversial (Hemelrijk et al., 1999).
A similar controversial topic is whether females choose males on the
basis of their parental abilities (Hrdy, 1981; Keddy-Hector, 1992). Getting
help in offspring provisioning would be beneficial, but even in species such as
callithrichids, in which direct male parental care is pronounced and appears
to limit female RS (Garber, 1997), it is unclear whether females preferentially choose males that signal their motivation to help (Price, 1990, 1992;
Tardif and Bales, 1997; van Schaik and Paul, 1996/1997). In any case, since
direct male assistance in offspring provisioning is rare in primates, the malecare hypothesis appears to have little general validity. However, even in
species characterized by negligible male parental care, such as vervets, females appear to prefer males that direct friendly behaviors toward their,
and other females’, offspring (Keddy-Hector, 1992). Moreover, males that
did not mate with an infant’s mother appear to be more likely to commit
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infanticide (Soltis et al., 2000), while putative or actual fathers are much
more likely to protect their offspring from infanticidal males (Borries et al.,
1999a,b). Clearly, any behavior that lowers the risk of infanticide would be
highly beneficial for female primates vulnerable to infanticide, and several of
their mate choice decisions appear to be consistent with this interpretation.
Physically superior and dominant males are most capable of protecting their
offspring against infanticidal attacks, and novel males or males that rise in the
dominance hierarchy are most likely to commit infanticide. Moreover, the
infanticide-avoidance hypothesis appears to be the most likely explanation
for polyandrous mating.
Direct benefits also appear to explain male mating decisions. Both experienced, parous females and high-ranking females often have a higher
reproductive rate, and offspring that are more likely to survive (Paul, 1998),
suggesting that preferences for these females are beneficial. Moreover, if
daughters inherit their mothers’ ranks and sons of high-ranking females
achieve higher reproductive success than sons of lower-ranking females
(Gerloff et al., 1999: bonobos; Paul et al., 1992: Barbary macaques; Smith
and Smith, 1988: natal rhesus macaques; van Noordwijk and van Schaik,
1999: long-tailed macaques), males also gain a long-term direct benefit from
choosing dominant females. Finally, savannah baboons also provide strong
evidence that males obtain direct benefits by choosing females with large
swellings because they produced a larger number of offspring per year and
their offspring were also more likely to survive (Domb and Pagel, 2001).
To conclude that indirect, genetic benefits are not involved in mate
choice decisions of primates would be premature. In fact, there are several
lines of evidence for indirect benefits. Incest avoidance provides the most
obvious example. By choosing unrelated males, females avoid deleterious
effects of close inbreeding (Pusey and Wolf, 1996), maintain heterozygosity
(Brown, 1997), and may avoid genetic incompatibility (Zeh and Zeh, 1996).
Moreover, since the potential costs from close inbreeding would be much
higher for the sex with the lower potential reproductive rate it is not surprising that females are more responsible for avoiding incestuous matings
than males are (Manson and Perry, 1993; Soltis et al., 1999). Further evidence for genetic benefits comes from laboratory breeding data on pig-tailed
macaques, in which offspring survival was strongly associated with paternal
genes (Sackett, 1990). Further research with the colony showed that parental
MHC antigen sharing predicted >70% of pregnancy loss among pairs with a
poor reproductive history (Knapp et al., 1996). The data support the notion
that free female mate choice yields important fitness benefits for mothers,
and the fitness differentials between offspring produced by preferred versus nonpreferred males might even be underestimated in laboratory settings
(cf. Drickamer et al., 2000). Finally, the finding of Domb and Pagel (2001)
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that female sexual swellings are reliable signals of their long-term reproductive value and thus perhaps an index of a female’s heritable reproductive
quality means that males also potentially derive indirect benefits from mating
females with larger swellings.
Why Is Polyandrous Mating so Common in Primates?
Long before ornithologists noticed frequent extrapair fertilizations
among socially monogamous birds, primatologists wondered why female
primates engage in so many copulations with multiple males (Hrdy, 1981;
Taub, 1980). In fact, in almost all primate species females engage in multiple
matings with more than one male (van Noordwijk and van Schaik, 2000),
suggesting that fertilization is not the sole function of copulation. There
are optional hypotheses to explain the incidence of polyandrous matings
in primates. Extrapair matings in pair-living gibbons (Palombit, 1994; Reichard, 1995), titis (Mason, 1966) and fat-tailed dwarf lemurs (Fietz et al.,
2000), or extragroup fertilizations in chimpanzees (Gagneux et al., 1997; but
see Constable et al., 2001) and other species (Berard et al., 1994; Ohsawa
et al., 1993) might be explained by the good-genes hypothesis, if the females
were paired with genetically inferior partners. However, strong empirical
evidence in support of this hypothesis is still lacking in all these cases. Moreover, models based on indirect (genetic) benefits clearly do not provide a
general explanation for the incidence of polyandrous mating in primates,
because they cannot explain the evolution of prolonged periods of female
sexual activity and copulations outside the conceptional period in anthropoid
primates (Martin, 1992). For the same reason, the fertility-insurance hypothesis (Small, 1993) is an unlikely explanation for the incidence of polyandrous
matings in primates, which appears to be true even in prosimians, which have
very short mating periods (Brockman and Whitten, 1996). What other direct
benefits might female primates accrue from polyandrous matings?
In some species, e.g., chimpanzees and bonobos, females at least sometimes appear to trade sex for food (Stanford, 1999; but see Hemelrijk et al.,
1999). But the ‘prostitution hypothesis’ (Symons, 1979) does not provide a
general explanation for polyandrous mating, because food sharing is rare,
and polyandrous mating is common among primates. Similarly, the additional male-care hypothesis does not apply to all primates, since males of
most primate species are not strongly involved in routine daily care of young
(Whitten, 1987). For the same reason the ‘ménage-à-trois’ scenario (Enquist
et al., 1998; Rodrigues-Gironés and Enquist, 2001), in which females are hypothesized to secure more male assistance by attracting other males and
thereby influence their own mates to stray less, appears to have little explanatory value for most primates (pair-living primates with male care are
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an obvious possible exception). However, both the additional male-care and
the ménage-à-trois hypotheses might explain the evolution of polyandrous
mating in species such as callithrichids, in which mothers appear to rely on
the help of males for successful reproduction (Garber, 1997). Females may
also mate polyandrously in order to deplete the amount of sperm available
for other females (Small, 1988) or to avoid costs from rejecting copulation
attempts by males. However, these explanations, too, appear to have limited explanatory power: The first scenario would induce a strong selection
pressure on males to produce more sperm (van Noordwijk and van Schaik,
2000), and the latter assumes that most, if not all copulations are initiated
by males and only accepted by essentially coy females, which is not the case
(Hrdy, 1986; Smuts, 1987).
A simple, though rarely considered possibility is, of course, that females
“just wanna have fun” (Small, 1993). According to this argument, polyandrous mating would be a nonadaptive byproduct of a strong motivation to
seek sexual pleasure, which ultimately evolved to ensure fertilization. For
two reasons, this explanation is unlikely. First, polyandrous sexual behavior
is costly, suggesting that there must be some more rewards than pure psychological well-being. And second, there is strong evidence that there are
such rewards.
More than 20 years ago, Hrdy (1979) speculated that polyandrous mating may serve to confuse paternity and, thereby, to reduce the risk of infanticide by males. The hypothesis eventually received substantial indirect
and direct empirical support. Strong indirect support for the infanticideavoidance hypothesis comes from a comparative analysis of mammalian
sexual behavior patterns by van Noordwijk and van Schaik (2000), who
found that, especially among carnivores and primates, polyandrous mating
is far more common in species vulnerable to infanticide than in nonvulnerable species: vulnerability to infanticide measured by the lactation/gestation
length ratio (van Schaik, 2000a,b). Other characteristics of female sexual
activity patterns such as the length of mating periods and the incidence of
postconception mating provide further support for the infanticide-avoidance
hypothesis (van Noordwijk and van Schaik, 2000).
The most compelling direct evidence that polyandrous mating reduces
the risk of infanticide comes from a study on Japanese macaques in which
infanticide occurred and males attacked infants of nonmates 8 times more
often than infants of former mates (Soltis et al., 2000). Although it might be
argued that the researchers missed the majority of copulations during the
preceding mating season, the data are remarkably consistent with several
other studies showing that fathers or possible sires virtually never attack their
own offspring. Chimpanzees are a possible exception (Hiraiwa-Hasegawa
and Hasegawa, 1994). Males actively defend their actual or putative offspring
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against infanticidal males (e.g. Borries et al., 1999a,b; reviewed by Paul et al.,
2000).
These data also show the female’s dilemma, however: she should concentrate paternity with the male most capable of protecting her offspring
against infanticidal attacks, but she also would benefit from confusing paternity by mating polyandrously in order to reduce the risk of infanticide (van
Schaik et al., 2000). Apparently, the evolution of prolonged follicular phases
and unpredictable ovulations (van Schaik et al., 2000), as well as signals
advertising female reproductive state such as sexual swellings (Domb and
Pagel, 2001; Nunn, 1999; Zinner and Deschner, 2000) and copulation calls
(Semple and McComb, 2000), which attract the most dominant males, serve
as a solution of the dilemma. They allow females to manipulate paternity
by concentrating it largely with top dominant males, while still confusing
it to the extent that other, potentially infanticidal males occasionally sire
offspring (van Schaik et al., 2000).
In conclusion, there is strong evidence in support of the hypothesis that
females gain direct fitness benefits from polyandrous mating. The protection against infanticide by males hypothesis received substantial support
from both comparative analyses and empirical observations and appears
to provide the explanation with the widest application. Whether this hypothesis also explains extrapair matings in pair-living primates such as gibbons, or whether such cases are better explained by indirect benefits, are
unproven. Moreover, protection against infanticide is clearly not the only
function of polyandrous mating in primates. In callithrichids, which are
not vulnerable to male infanticide (van Noordwijk and van Schaik, 2000),
polyandrous mating requires another explanation, and the additional male
care hypothesis appears to be a likely alternative (Soltis and McElreath,
2001).
Is There Evidence for Cryptic Female Choice in Primates?
Whether females can influence paternity through cryptic female choice
(Eberhard, 1996) is much-debated (Birkhead and Møller, 1998; Cunningham
and Birkhead, 1998). Cryptic female choice requires that they mate polyandrously, which is clearly the case in many primates (van Schaik, 2000; van
Noordwijk and van Schaik, 2000). Moreover, there is good evidence that
polyandrous matings are advantageous for females. These benefits do not
appear to be genetic, however; afterall in most anthropoids a large proportion of copulations occurs outside the female’s ovulatory period, making
it unlikely that sperm selection is involved. Female control over paternity
may nonetheless be common in primates, and exaggerated female sexual
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swellings may provide the most telling example (Dixson and Mundy, 1994).
Typically, swellings peak during the time when ovulation is most likely, and
males usually compete most intensely for females that are maximally swollen
(Dixson, 1998, Domb and Pagel, 2001). Accordingly, sexual swellings, appear
to function as honest signals of female fertility (Nunn, 1999; Domb and Pagel,
2001).
Prominent sexual swellings may make it quite difficult for males to deposit their sperm near the cervix, and there is evidence that male chimpanzees
differ in their ability to fertilize the eggs of maximally swollen females
(Dixson and Mundy, 1994). By lengthening the genital tract, females seem to
be able, therefore, to exert control over which males fertilize their eggs. The
fact that exaggerated sexual swellings are typically found in multimale social
systems (Clutton-Brock and Harvey, 1976; Dixson, 1983; Nunn, 1999) is consistent with this interpretation. Yet, although it seems reasonable that this
type of sperm selection influenced the evolution of male genital morphology, two caveats are needed: First, it is still unclear how females benefit from
differential selection of sperm in this case (cf. Cunningham and Birkhead,
1998), and second, there are good reasons to assume that female sexual
swellings evolved for some other reasons than sperm choice (Domb and
Pagel, 2001; Nunn, 1999). Accordingly, cryptic female choice would only be
a by-product of the evolution of sexual swellings.
CONCLUSION
After a long time sexual selection theory lay dormant, the crown jewel
of Darwin’s theories eventually received substantial support from a rich
variety of both theoretical and empirical studies. Primatologists were long
aware that non-human primates have preferences for certain mating partners, but until recently the functions and evolutionary consequences of such
preferences remained obscure. This situation seems to be different today,
but even now many questions remain to be answered, and some fields are
virtually neglected. The evolution of similar display structures in males and
females, such as the scarlet face of the bald uakari or the moustache of the
emperor tamarin are an example. Darwin found it “scarcely conceivable that
these crests of hair, and the strongly contrasted colours of the fur and skin,
can be the result of mere variability without the aid of selection; and it is
inconceivable that they can be of use in any ordinary way to these animals.
If so, they have probably been gained through sexual selection” (Darwin,
1998, p. 569). According to modern sexual selection theory, such ornaments
are likely to result from mutual mate choice and should occur most often
in species where males and females have similar parental roles and the sex
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ratio is close to unity (Andersson, 1994). Emperor tamarins, as well as many
other callithrichids, appear to meet this prediction, but systematic analyses
are still lacking.
I have begun this review with Darwin’s account of the brightly colored
male mandrill, and likewise I will end. In Primate Sexuality, Dixson (1998,
p. 195) noted that “it is entirely possible that a male’s ability to develop and
maintain these brightly coloured structures signals his health and vitality, his
ability to tolerate parasites (Hamilton and Zuk, 1982), or to advertise his
‘good genes’ by producing a costly advertisement (such as one which might
increase risk of predation: Zavahi, 1975).” Indeed, the sex skin color of male
mandrills is a condition-dependent trait which is associated with male age,
rank, plasma testosterone levels, testis size and rump fattedness (Setchell
and Dixson, 2001a,b; Wickings and Dixson, 1992). Moreover, low-ranking,
non-fatted males not only tend to have much paler sexual skin than that of
fatted dominant males but also achieve much lower mating and reproductive
success than the latter (Wickings et al., 1993).
Nevertheless, whether the brightly colored face of male mandrills is the
result of female choice, as Darwin believed and which seems “entirely possible” today, remains unproven. An alternative explanation is that the display
is more important in intermale communication. In fact, Wickler (1967) suggested that the signal function of the mandrill’s face lies in its “demoralizing
effect” on possible rivals (Wickler, 1967, p. 120). More recently, Setchell
and Dixson (2001a, p. 120) used the same argument, speculating that these
“extravagant sexual adornments may serve to advertise the quality of males
to one another, and therefore to reduce the probability of escalated agonistic
interactions between males” (Setchell and Dixson, 2001b; cf. Dixson, 1998).
Such an effect has recently been demonstrated in vervets, in which males differ markedly in scrotal color and males with similar scrotal color were more
antagonistic towards each other than males differing in color (Gerald, 2001).
Therefore, badges of social status may function to settle potentially costly
conflicts; but obviously, this does not exclude the possibility that they also,
and perhaps primarily, evolved to advertise the bearer’s quality to potential
mates. Indeed, whether female vervets or female mandrills also attend to
color differences among males is unknown. The required experiments have
simply not yet been conducted.
ACKNOWLEDGMENTS
This paper benefited greatly from discussions with, and comments from,
Uta Skamel. I am most grateful to Peter Kappeler and Dario Maestripieri
for inviting me to contribute to this special issue of IJP, to Sue Boinski, Peter
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Kappeler, Dario Maestripieri and an anonymous referee for constructive
comments on the manuscript, and to Joseph Soltis for access to unpublished
material.
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