Primate sexual swellings as coevolved signal systems

PRIMATES,41(1): 1-16, January 2000

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Primate Sexual Swellings as Coevolved Signal Systems ROBERT R. STALLMANN and JEFFERYW. FROEHLICH University of New Mexico

ABSTRACT. Many female catarrhine primates possess visually conspicuous organs that apparently function to increase the sexual interest of adult male conspecifics around the time the female is ovulating - i.e, sexual swellings. The hypothesized functional benefits for both sexes of these sexual swellings are reviewed (honest signaling; paternity confusion; paternity confidence and paternal investment; protection; incitement of precopulatory male-male competition; and postcopulatory sexual selection), as well as an additional hypothesis that has not yet been applied to this problem (sensory exploitation). Currently available evidence is presented that supports or fails to support each of these hypotheses. Predictions associated with broad groupings of these hypotheses, which could be tested in noninvasive field studies, are then presented. Ecological circumstances are discussed that could have led to differential mating success among female primates, and hence to sexual selection on females and directional evolution of sexual swellings. It is concluded that the available evidence does not support the paternity confidence-paternal investment hypothesis; that the paternity confusion hypothesis lacks empirical support, but could still be viable; and that insufficient data exists at present to rigorously test the other hypotheses. The ecological factors that may have led to differential reproductive success among females as a function of mating frequency or mate choice likewise require further empirical investigation. Key Words: Sexual swellings; Sexual conflict; Sexual selection; Mate choice; Multiple mating.

INTRODUCTION Female Old World primates may have evolved large, brightly-colored "sexual swellings" independently up to five times, since different tissue areas are involved within each of these clades (DIxsoN, 1998a). The form of sexual swellings can also be highly variable even among closely-related species and subspecies (Fig. 1). While non-adaptive hypotheses of sexual swelling evolution have been proposed, none of these is convincing (DIxSON, 1998a), and the markedly sexually arousing effect of sexual swellings on male conspecifics, independent of olfactory or behavioral cues (BIELERT& ANDERSON, 1985), together with temporal bracketing of ovulation (WlLOT et al., 1977), strongly suggest their adaptive nature and their function, in the broadest possible sense: the attraction of one or more males for mating. However, the question of why and how sexual swellings evolved, and precisely what they do, remains unanswered. The present moment happens to be an excellent time for primatologists to attempt resolution of this problem, since behavioral ecologists have very recently begun to investigate such processes as male mate choice, female competition for mates, sperm limitation, the effect of offspring survival on female fitness, and the effects of sexual selection on females, which were only recently considered very unlikely on theoretical grounds (CuNNINGHAM & BmKHEAD, 1998; EBERHARD, 1998; cf. ALTMANN, 1997). This trend is creating the opportunity for interdisciplinary cross-fertilization between primatologists and behavioral ecologists specializing in other taxa, principally arthropods and birds.

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Among the proposed adaptive benefits of sexual swellings are honest signaling of female quality (PAOEL, 1994), incitement of agonistic male-male competition (CLuTrON-BROCK & HARVEY, 1976), paternity confusion (HRDY, 1981), a "bodyguard" hypothesis (NuNN, 1996), increased paternity confidence and paternal investment (HAMILTON,1984), and postcopulatory sexual selection (HARVEY & MAY, 1989). In addition to the aforementioned hypotheses, sensory exploitation (RYAN et al., 1990) may be worthy of consideration as well, from the male perspec-

Evolution of Sexual Swellings

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tive. We will, of course, also consider the evolution of proceptive sexual behavior (BEACH, 1976) and either mate choice or multiple mating in female primates when discussing the evolution of sexual swellings, since these behaviors most likely work with sexual swellings as a functional unit. Most of the functional hypotheses that have been invoked to explain the evolution of sexual swellings have implicitly examined the function of sexual swellings in relation to the female's evolutionary interests (CLUTTON-BROCK& HARVEY, 1976; HRDY, 1981; HARVEY& MAY, 1989; NUNN, 1996). While this is understandable, since sexual swellings are a female trait, coevolutionary relationships such as that between the sexes may involve inherent conflict (e.g. ARNQVIST & ROWE, 1995; MANSON, 1997), and thus the interests of both parties need to be accounted for. Two authors (PAGEL, 1994; HAMILTON, 1984), in fact, have speculated about possible functional benefits for both sexes. In this paper, we will review the proposed benefits of female sexual swellings to both sexes, and summarize the evidence that currently exists for each. We will then list the predictions of two broad groups of hypothesized functions of sexual swellings. We will also explore the circumstances that could conceivably have led to differential mating success among female primates and, ultimately, to the evolution of conspicuous secondary sexual characters in females a phenomenon that is most unusual among animals in general, and particularly among mammals (ANDERSSON, 1994).

THE PROPOSEDADAPTIVEBENEFITSOF SEXUALSWELLINGS

Honest Signaling of Female Quality to Males ZAHAVI (1975) proposed that the "honesty" of a signal, or its reliability as an indicator of quality, can be maintained by the signal's costliness; that is, only individuals of high quality will be able to produce such signals (see also JOHNSTONE, 1995). Later, ZAHAVI'Smodel was modified somewhat to include the possibility of "condition-depe, ndent indicator traits" that are expressed only in individuals of higher fitness or viability; and "revealing indicator traits," the expression of which could serve as an indication of the signaler's health (ANDERSSON, 1994). Signals of immunocompetence (HAMILTON& ZUK, 1982) are one example of the latter. PAGEL (1994) argues, with the aid of a mathematical model, that males are expected to compete for any given female only to a limited degree; too much mating effort expended on behalf of any one female, within the context of a multi-male mating system, could cause him to lose out in the long run. By investing excessively in current reproduction, he could jeopardize his lifetime reproductive success. Better, argues PAGEL,to devote an optimal level of mating effort to each female. Such a strategy might well lead to the evolution of male mate choice, since some females might vary in phenotypic quality, and thus in their potential value to the male as mates. Therefore, the potential benefit to males of being able to detect differences in phenotypic quality among females could lead to selection for honest signals of female phenotypic quality hence the evolution of sexual swellings. Of course, the tradeoff between present and future reproduction need not be the only basis for male mate choice; a male may also have reason to be relatively selective if the quality of his ejaculate varies with the amount of time elapsed since his last mating (BIRKHEADet al., 1995), or if a given female's recent mating behavior affects her reproductive value (SCHWAGMEYER& PARKER, 1990). However, it should be mentioned that since PAGEL'Smodel focuses on benefits to the male, his hypothesis should not be considered an alternative to the other hypotheses reviewed here, which are primarily concerned with fitness benefits to females.

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R.R. STALLMANN& J. W. FROEHLICH

At present, there is little evidence that the size, color brightness or other characteristics of primates' sexual swellings are correlated with female phenotypic quality. However, a recent study of Japanese macaques (Macaca fuscata) suggests that sexual swellings may provide males with an indication of a female's nutritional status (MORI et al., 1997). Still, much more empirical investigation of the phenotypic correlates of sexual swelling size, shape, and color intensity is needed.

Paternity Confidence or Confusion? Based on the occurrence of infanticide among many species of primates (HIRAIWAHASEGAWA,1988), and the theory of kin selection, HRDY (1981) proposed adaptive paternity confusion as a possible female strategy leading to the evolution of sexual swellings and polyandrous or proceptive sexual behavior. HRDY (1981) argued that males represent a danger to female primates' reproductive interests; they may physically harm or frighten the females themselves (e.g. MANSON,1992, 1994; SMUTS, 1985). This could possibly lead to spontaneous abortion, infant death or other kinds of reproductive dysfunction (ALBERTSet ai., 1992). Or a male may kill the female's offspring (HRDY, 1979), thus causing her to resume ovarian cycling almost immediately. A male who is certain that he did not father the female's suckling infant would gain nothing, in terms of inclusive fitness, by waiting until the infant is weaned and lactational amenorrhea ends; better, from his point of view, to simply kill the infant. The female then has no adaptive "choice" but to resume cycling (any other strategy would cause an increased interbirth interval and reduced reproductive success), thus giving the male the opportunity to impregnate her. Therefore, it could certainly be argued that males, particularly new and unfamiliar males, represent a danger to females' evolutionary interests. While infanticide rates are probably higher in uni-male than in multi-male species, especially when the total amount of time spent observing each species is considered (HIRAIWA-HASEGAWA, 1988), females in uni-male groups do not have the option of mating with multiple males, and may therefore be unable to reduce the rate of infanticide. One must also consider that, as with predation, the risk of infanticide is a far more relevant consideration than is the rate (HILL& DUNBAR,1998), though risks are difficult to measure. For example, the lower rate of infanticide in multi-male species could be explained by the success of females at using multiple mating as a means of reducing the probability of infanticide (through paternity confusion), while the risk of infanticide nonetheless remains high. However, the lower rate of infanticide in multi-male species could still reflect a lower risk of infanticide in these species, since the reproductive payoff of infanticide for immigrant males living in multi-male groups is expected to be lower than that of immigrant males living in uni-male groups. A female in a multi-male group could mate with any number of other males in the group, and easily avoid mating with the infanticidal, immigrant male. Likewise, among chimpanzees (Pan troglodytes), there is no evidence that females whose infants are killed by males from other groups (accounting for about half of all infanticides by males in this species) subsequently transfer to the infanticidal male's group, or mate with him (HIRAIWA-HASEGAWA,1988). Thus, the difference in the reproductive payoff of infanticide for males based on the number of males in a group can explain the difference in infanticide rate between uni- vs multi-male groups as well as could the successful employment of a female counterstrategy, such as multiple mating. But why, then, do male chimpanzees kill infants? In chimpanzees, infanticide seems to occur as an incidental by-product of aggression against adult females by extra-group males: infants are usually not targets of aggression and are often allowed to escape (GOODALL,1986). It should also be remembered that, if multiple mating by females is an effective strategy for

Evolution of Sexual Swellings

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preventing infanticide, infanticide risk (measured in terms of male aggression toward infants), male investment in infants (including protection), and so on should be responsive to the male's mating history with the infant's mother. In rodents, there is very good evidence that males track their probablility of paternity effectively: if a male has mated with a female at precisely the right time, he may invest in her offspring; if he has not, he frequently kills them (PERR1GOet al., 1990; WOODROFFE & VINCENT, 1994). Female rodents' strong tendency to spontaneously abort in the olfactory presence of unfamiliar males likewise provides physiological corroboration for such paternity-tracking in rodents. The behavioral evidence for paternity-tracking in the more vision-dependent primates, however, is equivocal, and there is a concomitant lack of physiological evidence (WOODROFFE& VINCENT, 1994). In chimpanzees, for example, males may kill the infants of females with which they have copulated at around the time of conception (HIRAIWAHASEGAWA & HASEGAWA, 1994), while similar behavior does not seem to occur in house mice (Mus domesticus: PERRIGO et al., 1990). If females can use multiple mating as a strategy to reduce the risk of infanticide, then having mated with a female at around the time of conception should reliably prevent a male from killing her offspring. HAMILTON(1984) has proposed another possiblility for female advertising: she may increase her attractivity via a sexual swelling to attract and then mate with a single male, who, thus assured of his paternity of the offspring, might then preferentially invest in them. HAMILTON'S hypothesis therefore predicts both monandry and selective male paternal investment. The former prediction, however, runs counter to evidence suggesting that females in species with sexual swellings often mate polyandrously; female Barbary macaques (Macaca sylvanus), for example, are highly polyandrous (SMALL, 1989), yet have very large sexual swellings. More generally, female primates living in multi-male groups, who are likely to mate with multiple males during each estrous cycle, are far more likely to have sexual swellings than females living in uni-male groups, who cannot mate with multiple males (SILLEN-TULLBERG& MOLLER, 1993, Table 1; DIXSON, 1998a). One might also ask why, if sexual swellings function to increase individual males' paternity confidence, the duration of maximal swelling is so long in some species (e.g. Macaca nemestrina, 10 days: OI, 1987; Macaca tonkeana, 13 days: THIERRVet al., 1996a; Pan troglodytes, 1 2 - 1 3 days: WRANGHAM, 1993; Pan paniscus, 23.5 days: DAHL, 1986), and why the timing of ovulation can be variable with respect to the onset and termination of maximal turgescence (Wnrr'rEN & RUSSELL, 1996). While males probably do not rely solely on sexual swellings to gain information about the timing of ovulation, it is clear that swellings can be of only very limited help in determining the best time to mate with a female. NUNN (1996) has proposed a similar hypothesis, in which females use sexual swellings to increase the proximity of a dominant male, thus preventing harassment from conspecifics; this hypothesis, however, does not seem to depend on the dominant male's paternity certainty necessarily being increased. NUNN'S bodyguard hypothesis predicts that females should use their sexual swellings to attract dominant males, and to maintain such proximity outside of a strictly sexual context if possible. Therefore, secondary sexual characters in females that allow for continuous attractivity, such as the breasts and buttocks of human females (DIXSON, 1998a), might be particularly useful under such circumstances. There is some evidence for female choice for males of high dominance rank, although the evidence is often contradictory for the same species (SMALL, 1989; MANSON, 1992). However, substantial evidence also exists suggesting an absence of such choice, or even choice for lower-ranking males (SMUTS, 1987a; MANSON, 1992; OI, 1996). Methodological problems can be quite serious as well; for example, females' mating with subordinate or extragroup males may be undersampled in studies based only upon behavioral observation, due to the clandestine nature of such behavior (GAGNEUX et al., 1997), or the reduced habituation of

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R . R . STALLMANNt~c.ZJ. W. FROEHLICH

males from neighboring groups. During a howling battle between a habituated and an unhabituated troop, for example, one of us (JWF) witnessed a mating between a marked female howling monkey (Alouatta palliata) and a strange male, presumably from the opposing troop. Likewise, methods of behavioral observation vary greatly, and certain of these, such as behavioral sampling of males rather than females, may lead to doubtful conclusions of female choice for dominant males if females engage in extra-group or sneaky mating. Finally, patterns of differential reproductive success among males do not necessarily indicate female choice, nor does the choice to mate with a given male necessarily reflect an underlying preference for that male, due to the effects of mate-guarding by males (MANSON, 1997), sexual intimidation of subordinate males by dominant males (ESTEP et al., 1988; Ol, 1996), and male intimidation of females (SMUTS, 1987a). Therefore, data on "consortships" among primates are not useful for assessing female mating preferences, unless it is known which sex is more responsible for maintaining proximity (see MANSON, 1992, 1994, 1997, for recent attempts to disentangle female and male mating strategies in free-ranging primates).

Do Sexual Swellings Incite Precopulatory Male-male Competition ? One of the longest-standing explanations for the existence of sexual swellings is that they serve to facilitate or increase male-male agonistic competition for females, thus ensuring that the "best" male - with the best genes, perhaps - wins the competition (CLUTTON-BROCK& HARVEY, 1976; COX & LEBOEUF, 1977; WATSON, 1990). The agonistic-incitement hypothesis assumes that the male who wins the competition for mating access will be the one the female would have chosen to mate with. Female mating preferences can be quite independent of the results of male-male competition, however (QVARNSTROM & FORSGREN, 1998) and females often actively choose to mate with lower-ranking males, or at least attempt to do so (SMUTS, 1987a; MANSON, 1992; OI, 1996). This is problematic for the agonistic-incitement hypothesis, as it is for HAMmTON'S(1984) paternity confidence hypothesis.

Postcopulatory Sexual Selection, Multiple Mating, and Genetic Benefits Female primates may use sexual swellings to help them mate with multiple males, which can lead to postcopulatory sexual selection, and can ultimately increase the female's fitness, often by increasing that of her offspring. As in precopulatory sexual selection, both intrasexual and intersexual selection are possible. In polyandrously mating species (i.e. species in which females mate with multiple males; see ROLDAN t~z GOMENDIO,1995), sperm from various males competes for the chance to fertilize the female's ovum (BIRKHEAD,~ M~LLER, 1998a). The larger testes (HARCOURT,1995) and seminal vesicles (DIXSON, 1998b) of primate species that normally live in multi-male groups provide morphological evidence for the importance of sperm competition - and the presence of multiple mating by females - in these species. Likewise, females may exercise "cryptic" choice after insemination (EBERHARD,1996; OLSSON et al., 1996). The pre-mating "solicitation calls" given by females of some multiply-mating primate species that also have sexual swellings also provide evidence for the importance of either paternity confusion or postcopulatory sexual selection, rather than incitement of agonistic, precopulatory male-male competition, in shaping female primate phenotypes (Papio hamadryas: O'CONNELL & COWLISHAW, 1994; COWLISHAW • O'CONNELL, 1996; Macaca tonkeana: THIERRYet al., 1996b), since the agonistic-incitement hypothesis is better supported

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by the occurrence of calls given by females during copulation, especially in the initial stages of copulation (Cox & LEBOEUF, 1977). Thus, in these species, sexual swellings, solicitation calls, and proceptive sexual behavior may function in concert to recruit multiple mating partners. Collecting ejaculates from a number of male mates may be beneficial to female animals in a number of ways. Such multiple mating may increase the probability that the female's ovum will be fertilized (the fertility insurance hypothesis), provide nutrients to the female, promote genetic diversity among her offspring, lead to a more genetically compatible male fertilizing her egg, increase the sperm-competitive ability of her male offspring (the "sexy sperm" hypothesis: HARVEY & MAY, 1989; CURTSINGER, 1991), or increase the viability of offspring of both sexes (the "good sperm" hypothesis: YASUI, 1997; most hypotheses reviewed in BIRKHEAD & M~LLER, 1998b). Some of these hypotheses can be ruled out a priori for primates, due to certain characteristics of mammalian or primate reproductive biology. Mammalian sperm, for example, does not contain any nutritious matter that can be consumed or used by females, so this hypothesis can be eliminated for primates (GOMENDIOet al., 1998). Likewise, the genetic diversity hypothesis can be ruled out, since Old World anthropoid primates, the only primates that have sexual swellings, have offspring one at a time (FLEAGLE, 1999), and thus mating with multiple males within any given estrous cycle would not increase the genetic diversity of a female's offspring. (To increase the genetic diversity of her offspring, a female Old World primate would have to mate with multiple males over her lifetime, but not necessarily within any given estrous cycle. Mating with multiple males within estrous cycles could in fact reduce offspring genetic variability, if males vary in their sperm-competitive ability.) This leaves us with four possible mechanisms for increased female fitness: ferility insurance, genetic compatibi!ity, the sexy sperm hypothesis, and the good sperm hypothesis. According to the sexy sperm hypothesis, females whose ova are fertilized by males of superior sperm-competitive ability are more likely to have sons that likewise possess such ability, which will in turn prove successful in fertilizing many females, thus increasing the original female's number of grandoffspring (HARVEY8Z MAY, 1989). However, CURTSINGER(1991) has shown via mathematical modeling that heritable differences in sperm-competitive ability alone are unlikely to lead to the spread of multiple mating behavior among females in a population, unless this behavior is not at all costly (CuRTSINGER, 1991). Empirical evidence indicates that, in primates, multiple mating by females can indeed be quite costly in terms of aggression received from males (e.g. MANSON, 1992, 1994) and because of lost foraging time, since females' food intake affects their fitness (VANSCHA1K,1983). YASUI (1997) has modified the model presented by CURTSINGER(1991) such that the spermcompetitive ability of males is correlated with heritable general viability: hence the "good sperm" hypothesis. In such a situation, female multiple mating can spread within a population even if it is costly, because general viability is expressed in offspring of both sexes, while increased sperm-competitive ability only increases the fitness of male offspring (YASUI, 1997). Correlation of sperm-competitive ability with general viability can arise through ZAHAVI'S (1975) handicap mechanism (JOHNSTONE, 1995), wherein the costliness of sperm production limits the extent to which lower-quality males can allocate energy to it, thus causing sperm production to become an honest signal of overall male phenotypic quality. Good evidence for the costliness of sperm production exists for several animal species (DEwSBURY, 1982; VAN VOORHIES,1992; OLSSON et al., 1997). In addition, the large differences in allocation of tissue to sperm production among primate species, which seems to depend upon the likelihood of multiple mating by females (DIXSON, 1998b; HARCOURT,1995), and the difference in number of sperm per ejaculate and size of sperm reserves in monandrous vs polyandrous species (HARVEY& MAY, 1989; GOMENDIO et al., 1998), also suggest the costliness of

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R.R. STALLMANNt~ J. W. FROEHLICH

sperm production, since males that can avoid this cost (i.e. males in monandrous species) seem to do so. Furthermore, abundant evidence exists in many animal species that a male's genetic quality can affect the viability (e.g. growth or survival rates) of females' juvenile or adult offspring (REYNOLDS& GROSS, 1992; PETmE, 1994; PROMISLOWet al., 1998; WATSON, 1998); likewise, sperm quality and degree of inbreeding seem to be inversely related in at least one mammal species (ROLDAN et al., 1998). These genetic benefits often seem to be accrued by females who mate with multiple males, as evidenced in the positive relationship between the number of males with which a female mates, and the viability of her offspring (MADSEN et al., 1992; HOOGLAND,1998; WATSON,1998). An increased probability of genetic compatibility between male and female gametes, and thus a higher probability of offspring survival, is yet another possible benefit of multiple mating for female primates. The genetic compatibility hypothesis differs from the good-sperm hypothesis in that it does not depend upon an assumption of heritable variation in inherent male quality. The finding that a male's fertilization success depends upon the genotype of the female with which he mates in several nonmammalian species provides support for this hypothesis (OLSSON et al., 1996; WILSONet al., 1997; ZEH, 1997; CLARKet al., 1999); however, evidence for such an effect among mammals has not been found to date (CUNNINGHAMt~ BIRKHEAD,1998). On the other hand, immunological compatibility may be especially important in anthropoid primates, due to the great porosity of their placentas. While there is evidence that mating with multiple males modestly increases the probablility of conception (by 8%) in at least one mammal species, the same study also shows that litter size (and thus, perhaps, offspring viability) also increased as a function of the mother's number of sexual partners (HOOGLAND,1998). It is unclear, however, whether the selection pressure resulting from a slight increase in the probability of fertilization would be strong enough to favor the evolution of multiple mating and sexual swellings, especially among non-seasonally-breeding primate species.

Sensory Exploitation of Males by Females The German ethologist WOLFGANGWICKLER(1967) was one of the first writers to suggest the possibility that signals may evolve by taking advantage of pre-existing biases, leading to an evolutionary process now called sensory exploitation. WICKLER used this argument to explain the evolution of bare-skin rump patches, brightly colored scrotums and penises, and other conspicuous male traits in certain primates (WICKLER, 1967). RYAN and colleagues have studied sensory exploitation and pre-existing biases in tfingara frogs (Physalaemus pustulosus: RYANet al., 1990) and swordtail fish (Xiphophorus nigrensis: RYAN & WAGNER, 1987; X. helleri: BASOLO, 1990) -- that is, cases in which the signal bias of one sex may have evolved before the signal that seems to exploit it. Such pre-existing biases may be the result of either natural selection in other contexts (e.g. feeding) or could simply be an artifact of neural structure. Thus, the existence of a pre-existing bias (on the proximate, mechanistic level) in one sex can lead to exploitation of that bias (on the functional level) by the other sex. It is at least possible, then, that sexual swellings provide males with no useful information about female quality (although they probably provide some information about the occurrence of ovulation, excepting postconception Swellings). Such one-sided functionality can be explained only through the existence of a pre-existing bias in male primates. Two studies (PAGEL, 1994; CLUTrON-BROCK& HARVEY, 1976) have argued against the possibility that sexual swellings exploit pre-existing male sensory biases, on the grounds that males would inevitably have been selected to detect quality differences between females, or simply

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would not respond differentially to swellings o f different sizes at all. However, sensory exploitation cannot really be ruled out on selectionist grounds because selection may be constrained by a number of factors, chiefly the degree of selection pressure and the availability of variation in the relevant traits (GOULD & LEWONTIN, 1979). PREDICTIONS OF THE HYPOTHESES A number of the hypotheses reviewed above assume that females use sexual swellings to increase the odds o f their mating with a single high-quality male. These hypotheses include incitement of precopulatory male-male competition, paternity confidence/paternal investment, and the protection or bodyguard hypothesis. O f Course, when male quality and dominance are not well correlated, a female who mates with two males could still be pursuing a best-male strategy - that is, she might mate with the alpha male to avoid the cost of his aggression or to obtain his protection, while mating with one other high-quality male. However, this situation would arise only with regard to the paternity confidence/paternal investment hypothesis, since in the other two cases (incitement of precopulatory male-male competition, and use of males for protection), the "best male" should be the most dominant one. Another group of hypotheses presented here, including both postcopulatory sexual selection and the paternity confusion/infanticide avoidance hypothesis, assume that females use sexual swellings to mate with as many males as possible. Each of these two groups of hypotheses (the "best-male" vs "many-male" hypotheses: HRDY t~ WHIT]'EN, 1987) is logically associated with certain predictions, each of which is testable using observational data. We present the predictions for both groups of hypotheses in Table I. While it will be difficult to test the predictions of the various kinds of postcopulatory sexual selection, testing the infanticide-prevention hypothesis against the group of hypotheses that posit postcopulatory genetic benefits (sexy sperm, good sperm, and genetic compatibility) of multiple mating should not be too difficult, given appropriate methodology and sufficient data. In Table 2, we list the predictions of both of these groups of hypotheses. Predictions about infanticide rates were not included, because of the practical difficulty of obtaining such data,

Table 1. Predictions of the best-male and many-male groups of hypotheses. Best-male hypotheses Many-male hypotheses I. Individual females solicit three or more 1. Females solicit one male consistently, both among cycles for each female, males in each estrous cycle; among and among all femalesI) females, no consistent solicitation of particular males 2. Females mate consistently with one malet)

2. Females mate with three or more males per cycle

3. One male is consistently favored by females for furtive mating

3. No single male is consistently favored by all females for furtive mating

4. Contest competition among females for 4. Scramble competition among females for matings with the same male number of male mates per estrous cycle Best-male hypotheses include incitement of precopulatory male-male competition, the bodyguard hypothesis, and paternity confidence/paternal investment. Many-male hypotheses include paternity confusion/infanticide avoidance, and postcopulatory sexual selection. 1) Females pursuing a best-male strategy could also mate with the alpha male (to avoid his aggression, obtain his parental care for her offspring, etc.), as well as mating with one additional "high-quality" male (if male quality does not correlate well with dominance).

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Table 2. Predictions of the genetic benefits and paternity confusion/infanticide avoidance groups of hypotheses, in terms of expected correlations with female's number of mates per estrous cycle for females in multi-male groups. Parameter Genetic benefits Infanticide prevention Infant mortality --Juvenile mortality -0 Offspring adult fitness + 0 Aggression received by infant from males 0 Cycles to conception -0 Probability of abortion -0 Infant size or weight + 0 +: Positive; - : negative; 0: no correlation. Genetic benefits hypotheses include the sexy sperm, good sperm, and genetic and/or immunological compatibility hypotheses. Predictions of infanticide rates are excluded for both practical and theoretical reasons, as explained in the text. Dominance of the female must be controlled for in all cases, since dominance may correlate with both number of mates and food intake.

and the potential confounding of infanticide rate and infanticide risk (HILL 8z DUNBAR, 1998). If support is found for postcopulatory selection, then testing of more specific hypotheses within this category would be the appropriate next step. CONDITIONS LEADING TO DIFFERENTIALMATING SUCCESS AMONG FEMALES Most o f the hypotheses reviewed above point to some form of sexual selection on females as the likely cause of the evolution of sexual swellings in female primates; NUNN'S (1996) hypothesis is the apparent exception. By definition, sexual selection is caused by differential access to mates (i.e. access to either one high-quality male or several males) among individuals with different phenotypes. Regardless of the conceivable benefits of sexual swellings for female fitness, selection for larger, brighter or more elaborate swellings cannot proceed without variation in mating success (or success in attracting males, in the case of NUNN'S hypothesis) among females (e.g. HOOGLAND, 1998) as a function of swelling characteristics. Thus, as PAGEL (1994) has pointed out, the evolution of exaggerated sexual swellings probably implies competition among females for mates over evolutionary time, and a pattern of differential mating success among females throughout evoutionary history, as a function of swelling characteristics. O f course, such female-female competition for mates can and often does involve scramble competition rather than contest competition; thus fighting among females over male mates is not necessarily predicted, although it does occur (SMUTS, 1987a). More subtle competition over males, perhaps based on female-female harassment, is probably more widespread (GOLDFOOT, 1971; ZUMPE & MICHAEL, 1987, 1989), perhaps because all-out fighting would be too costly even for the aggressors. We have reviewed the various benefits that may accrue to females with more elaborate sexual swellings; now, we will enumerate the conditions that can lead to differential mating success among females (Fig. 2). OWENS and THOMPSON (1994) have argued that a large degree of variation in female quality can increase the likelihood of male mate choice, even in species (such as primates) in which the potential reproductive rate o f males is higher than that o f females. Dominance is one example of a means by which female phenotypic quality can vary, perhaps with consequences for the female's fecundity. More dominant females tend to be more fecund, for reasons that are at least partly independent of their mating success. For example, dominance seems to be associated with increased reproductive success in females only when food resources are located in defensi-

Evolution of Sexual Swellings

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Dire~ evo3 ofs swe Fitness ~ _ ~ benefitsof multiple mating

~

,nal on tal Lgs

Vari :e in fe le fi~ ss

Variation I in fern_,ale I

Male-male competition, intimidation, peripheralization

Sexualswelling ( characteristics

Fig. 2. Pathways leading to variance in female fitness based on access to males, and in turn to directional evolution of sexual swellings. OSR: Operational sex ratio, the number of breeding males per breeding female.

ble patches (HARCOURT, 1989; PUSEY et al., 1997). Likewise, the survival of female primates' offspring may be related to the quality of maternal care that the offspring receive, as well as the mother's nutritional condition (ALTMANN,1997). It is therefore not suprising that male primates often seem to prefer to mate with high-ranking females (GLIcK, 1980; PAUL, 1989; KUESTER& PAUL, 1996). Aside from differences in phenotypic quality among females, a number of other conditions can lead to mate choice by males. One of these conditions is sperm limitation. There is a growing consensus among many researchers that the cost of sperm production is not trivial, and that this cost may limit males' mating options (see the section above on postcopulatory sexual selection). The risk of sperm competition also has been shown to influence male mating decisions in some cases, and can lead to mate choice by males based on a female's recent mating history (SCHWAGMEYERt~ PARKER, 1990), or the amount of time elapsed since the male's last ejaculation (BIRKHEADet al., 1995). Likewise, if males must compete with other males for each additional female mate (on the agonistic, precopulatory level), males should then become more choosey about which females they will compete over (PAGEL, 1994). In either case, mate choice by males could lead to greater efforts by females to overcome males' reluctance to mate with them, possibly leading to the further enlargement or elaboration of sexual swellings. Intimidation of subordinate males by dominant males can also make it more challenging for a female to mate with multiple males; in many cases, subordinate males will not mate with females in the presence of the dominant male, in spite of the females' attempts to solicit the

12

R . R . STALLMANN& J. W. FROEHLICH

subordinate males (ESTEP et al., 1988; Ol, 1996). When subordinate males are moderately peripheralized due to intensified male-male competition (causing a female-skewed operational sex ratio), recruitment of multiple mating partners will be especially challenging for females, since peripheral males will be reluctant to mate when the dominant or central male is within sight (OI, 1996). When peripheralization of subordinate males becomes too great (as in onemale groups), the benefits to females of seeking multiple mating partners will be outweighed by the costs of search time and lost foraging time - hence the rarity of sexual swellings in primate species living in one-male groups (SILLEN-TULLBERG& MOLLER, 1993, Table 1).

CONCLUSIONS It is too early at this point to make firm decisions regarding the empirical support for most of the functional hypotheses discussed above, simply because theoretical discussions are far more abundant in the literature than empirical studies. Far more work must be done before we can substantially narrow the field of candidate hypotheses. However, we believe that HAMILTON'S (1984) hypothesis that sexual swellings serve to increase the paternity confidence of a single male can be rejected with a reasonable degree of confidence, for the reasons outlined above. While males in many primale taxa seem to have some information about the timing of females' ovulation (whether or not females of the species in question have sexual swellings: MANSON, 1997), it is clear that sexual swellings do a poor job of pinpointing the appropriate moment for mating - especially when one considers that female primates do not store sperm, and the effective lifetime of primate sperm is dwarfed by the duration of maximal swelling in most species (see above; GOMENDIOet al., 1998). The hypothesis that sexual swellings allow female primates to confuse paternity by mating with several males (HRDY, 1981) cannot be ruled out at present, but the empirical evidence that has been offered in support of it is not robust. Clearly, the occurrence of a few cases of infanticide within a given population or species does not necessarily indicate a high risk of infanticide for females of that species, nor that multiple mating is an effective counterstrategy. Likewise problematic is the lack of evidence of paternity-tracking by male primates (WoODROFFE,~Z VINCENT, 1994). Since sexual swellings seem to have evolved independently in the genus Pan (SILLEN-TULLBERG,~ MOLLER, 1993; DIXSON, 1998a), they could conceivably have a different function where this taxon is concerned. Far more quantitative data on both male behavior toward infants and female mating behavior are needed before conclusions can be made. NUNN'S (1996) bodyguard hypothesis cannot yet be ruled out either, again due to a lack of available data. It is important, however, to distinguish between possible benefits to females in theory, and benefits that could directly result from having a sexual swelling. The trouble with the bodyguard hypothesis is nearly the opposite of the problem with HAMILTON'S(]984) paternity-certainty hypothesis. In the former case, sexual swelling duration is too long for the proposed mechanism to work. In the latter case, one wonders why continuous attractivity would not have evolved in all the species concerned, rather than only in humans (DIxsoN, 1998a). Perhaps more importantly, the amount of aggression that is frequently directed by males against females in a sexual context - in species with and without sexual swellings (SMUTS, 1987b) -seems to weigh against an hypothesis that depends upon male protection. MANSON (1994) did find that rhesus macaque (Macaca mulatta) females are less likely to be harassed by another male when next to a dominant male, than they are when nearest to a subordinate. Females in this population still, however, sexually solicited and mated with subordinate males, despite the higher risk of harassment (MANSON, 1992, 1994).

Evolution of Sexual Swellings

13

Unfortunately, data sufficient to rigorously test many of the hypotheses that we have discussed do not yet exist. The same is true regarding conditions that allowed sexual selection on female primates to occur - for example, there is a very modest amount of information regarding male mate choice, but none regarding male mate choice for sexual swelling characteristics. There is even less information available on the long-term fitness consequences for females of male mate choice, sperm limitation, and so on. We believe, however, that the problem of how and why sexual swellings evolved is a tremendously important one - not only for primate or human evolution, but for our knowledge of the evolution of animal behavior in general - and that its eventual resolution will contribute greatly to our understanding of the processes of evolution.

Acknowledgements.We wish to thank B. C. CAMPBELL,A. H. HARCOURT,J. B. LANCASTER,A. J. SCHILLING, E. L. STALLMAN,and B. I. STRASSMANN,and three anonymous reviewers, who read drafts of the present paper, or an earlier version, and provided invaluable suggestions and comments.

REFERENCES

ALBERTS,S. C.; SAPOLSKY,R. M.; ALTMANN,J. 1992. Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Horm. Behav., 26: 167-178. ALTMANN,J. 1997. Mate choice and intrasexual reproductive competition: contributions to reproduction that go beyond acquiring more mates. In: Feminism and Evolutionary Biology: Boundaries, Intersections, and Frontiers, GOWATY,P. A. (ed.), Chapman & Hall, New York, pp. 320-333. ANDERSSON, M. 1994. Sexual Selection. Princeton Univ. Press, Princeton. ARNQVIST,G.; ROWE,L. 1995. Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proc. R. Soc. Lond. B, 261 : 123-127. BASOLO,A. L. 1990. Female preference predates the evolution of the sword in swordtail fish. Science, 250: 808-810. BEACH, E A. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm. Behav., 7: 105-138. BIELERT,C.; ANDERSON,C. M. 1985. Baboon sexual swellings and male response: a possible operational supernormal stimulus and response interaction, hzt. J. Primatol., 6: 377-393. BmKHEAD, T. R.; FLETCHER,E; PELLATT,E. J.; STAPLES,A. 1995. Ejaculate quality and the success of extra-pair copulations in the zebra finch. Nature, 377: 422-423. BmKHEAD,T. R.; MOLLER, A. P. (eds.). 1998a. Sperm Competition and Sexual Selection. Academic Press, New York. BIRKHEAD,W. R.; MOLLER,m. P. 1998b. Sperm competition, sexual selection and different routes to fitness. In: Sperm Competition and Sexual Selection, BIRKHEAD,T. R.: MOLLER, A. P. (eds.), Academic Press, New York, pp. 757-781. CLARK, A. G.; BEGUN,D. J.; PROUT, T. 1999. Female x male interactions in Drosophila sperm competition. Science, 283: 217-220. CLUTTON-BROCK,T. H.; HARVEY,P. H. 1976. Evolutionary rules and primate societies. In: Growing Points in Ethology, BATESON, P. P. G.; HINDE, R. A. (eds.), Cambridge Univ. Press, Cambridge, pp. 195-237. COWLISHAW,G.; O'CONNELL, S. M. 1996. Male-male competition, paternity certainty and copulation calls in female baboons. Anim. Behav., 51: 235-238. Cox, C. R.; LEBOEUF,B. J. 1977. Female incitation of male competition: a mechanism in sexual selection. Amer. Naturalist, 111: 317-335. CUNNJNGHAM, E. J. A.; BmKHEAD, T. R. 1998. Sex roles and sexual selection. Anim. Behav., 56: 1311-1321. CURTSINGER,J. W. 1991. Sperm competition and the evolution of multiple mating. Amer. Naturalist, 138: 93-102. DAHL, J. F. 1986. Cyclic perineal swelling during the intermenstrual intervals of captive female pygmy chimpanzees (Pan paniscus). J. Human Evol., 15: 369-385. DEWSBURY,D. A. 1982. Ejaculate cost and mate choice. Amer. Naturalist, 119:601-610.

14

R.R. STALLMANNt~ J. W. FROEHLICH

DIXSON, A. E 1998a. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Human Beings. Oxford Univ. Press, Oxford. DIXSON, A. F. 1998b. Sexual selection and evolution of the seminal vesicles in primates. Folia Primatol., 69: 300-306. EBERHARD, W. G. 1996. Female Control: Sexual Selection by Cryptic Female Choice. Princeton Univ. Press, Princeton. EBERHARD,W. G. 1998. Female roles in sperm competition. In: Sperm Competition and Sexual Selection, BmKHEAD,T. R.; MOLLER, A. E (eds.), Academic Press, New York, pp. 91 -116. ESTEP, D. Q.; NIEUWENHUHSEN,K.; BRUCE, K. E. M.; DE NEEF, K. J.; WALTERS,P. A.; BAKER,S. C.; SLOB, A. K. 1988. Inhibition of sexual behaviour among subordinate stumptail macaques, Macaca arctoides. Anim. Behav., 36: 854-864. FLEAGLE,J. G. 1999. Primate Adaptation and Evolution (2nd ed.). Academic Press, San Diego. GAGNEUX, E; WOODRUFF,D. S.; BOESCH,C. 1997. Furtive mating in female chimpanzees. Nature, 387: 358-359. GLICK, B. B. 1980. Ontogenetic and psychobiological aspects of the mating activities of male Macaca radiata. In: The Macaques: Studies in Ecology, Behavior and Evolution, LINDBURG,D. G. (ed.), Van Nostrand Reinhold, New York, pp. 345-369. GOLDFOOT,O. A. 1971. Hormonal and social determinants of sexual behavior in pigtail monkeys (Macaca nemestrina). In: Normal and Abnormal Development of Brain and Behavior, STOELINGA,G. B. A., VANDER WERFFTENBOSCH,J. J. (eds.), Leiden Univ. Press, Leiden, pp. 325-342. GOMENDIO, M.; HARCOURT,A. H.; ROLDAN, E. R. S. 1998. Sperm competition in mammals. In: Sperm Competition and Sexual Selection, BIRKHEAD,T. R.; MOLLER, A. P. (eds.), Academic Press, San Diego, pp. 667-756. GOODALL, J. 1986. The Chimpanzees of Gombe: Patterns of Behavior. Harvard Univ. Press, Cambridge, Massachusetts. GOULD,S. J.; LEWONT1N,R. C. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. B, 205:581-598. HAMILTON,W. D.; ZUK, M. 1982. Heritable true fitness and bright birds: a role for parasites? Science, 218: 384-387. HAMILTON,W. J. 1984. Significance of paternal investment by primates to the evolution of male-female associations. In: Primate Paternalism, TAUB, D. M. (ed.), Van Nostrand Reinhold, New York, pp. 309-335. HARCOURT, A. H. 1989. Environment, competition and reproductive performance of female monkeys. Trends Ecol. Evol., 4: 101 -105. HARCOURT,A. H. 1995. Sexual selection and sperm competition in primates: what are male genitalia good for? Evol. Anthropol., 4:121 -129. HARVEY,P. H.; MAY,R. M. 1989. Out for the sperm count. Nature, 337: 508-509. HILL, R. A.; DUNBAR, R. 1. M. 1998. An evaluation of the roles of predation rate and predation risk as selective pressures on primate grouping behaviour. Behaviour, 135:411-430. HIRAIWA-HASEGAWA,M. 1988. Adaptive significance of infanticide in primates. Trends Ecol. Evol., 3: 102-105. HIRAIWA-HASEGAWA,M.; HASEGAWA,Z. 1994. Infanticide in nonhuman primates: sexual selection and local resource competition. In: Infanticide and Parental Care, PARMIGIANI,S., VOMSAAL,E S. (eds.), Harwood, New York, pp. 137-154. HOOGLAND,J. L. 1998. Why do female Gunnison's prairie dogs copulate with more than one male? Anim. Behav., 55:351-359. HRDY, S. B. 1979. Infanticide among animals: a review, classification and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol., 1: 13-40. HRDY, S. B. 1981. The Woman That Never Evolved. Harvard Univ. Press, Cambridge, Massachusetts. HRDY,S. B.; WHITTEN,P. L. 1987. Patterns of sexual activity. In: Primate Societies, SMUTS,B. B.; CHENEY, D. L.; SEYFARTH,R. M.~, WRANGHAM,R. W.; STRUHSAKER,T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 370-384. JOHNSTONE,R. A. 1995. Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol. Rev., 7 0 : 1 - 6 5 . KUESTER, J.; PAUL, A. 1996. Female-female competition and male mate choice in Barbary macaques (Macaca sylvanus). Behaviour, 133: 763-790.

Evolution of Sexual Swellings

15

MADSEN, T.; SHINE,R.; LOMAN, J.; H.~KANSSON,T. 1992. Why do female adders copulate so frequently? Nature, 355: 440-441. MANSON,J. H. 1992. Measuring female mate choice in Cayo Santiago rhesus macaques. Anita. Behav., 44: 405-416. MANSON, J. H. 1994. Male aggression: a cost of female choice in Cayo Santiago rhesus macaques. Anita. Behav., 48: 473-475. MANSON, J. H. 1997. Primate consortships: a critical review. Cur. Anthropol., 38: 353-374. MORI, A.; YAMAGUCHI,N.; WATANABE, K.; SHIMIZU, K. 1997. Sexual maturation of female Japanese macaques under poor nutritional conditions and food-enhanced perineal swelling in the Koshima troop. Int. J. Primatol., 18: 553-579. NUNN, C. L. 1996. Male harassment and the evolution of prominent estrous advertisement in primates. Paper presented at the International Primatological Society, American Society of Primatologists Joint Congress, Madison, Wisconsin. O'CONNELL, S. M., COWLISHAW,G. 1994. Infanticide avoidance, sperm competition and mate choice: the function of copulation calls in female baboons. Anita. Behav., 48: 687-694. O1, T. 1987. Sexual behavior of the wild pig-tailed macaques in west Sumatra: Kyoto Univ. Overseas Res. Rep. Studies on Asian Non-human Primates, No. 6. Primate Res. Instit., Kyoto Univ., Inuyama, Japan. OI, T. 1996. Sexual behaviour and mating system of the wild pig-tailed macaque in West Sumatra. In: Evolution and Ecology of Macaque Societies, FA, J. E.; LINDBURG,D. G. (eds.), Cambridge Univ. Press, Cambridge, pp. 342-368. OLSSON, M.; MADSEN,Z.; SHINE,R. 1997. Is sperm really so cheap?: costs of reproduction in male adders, Vipera berus. Proc. R. Soc. Lond. B, 264: 455-459. OLSSON, M.; SHINE,R.; MADSEN,Z.; GULLBERG,A.; TEGELSTROM,H. 1996. Sperm selection by females. Nature, 383: 585. OWENS, 1. P. E; THOMPSON,D. B. A. 1994. Sex differences, sex ratios and sex roles. Proc. R. Soc. Lond. B, 258: 93-99. PAGEL, M. 1994. The evolution of conspicuous oestrous advertisement in Old World monkeys. Anita. Behav., 47:1333-1341. PAUL, A. 1989. Determinants of male mating success in a large group of barbary macaques (Macaca sylvanus) at Affenberg Salem. Primates, 30:461-476. PERRIGO, G.; BRYANT,W. C., VOM SAAL, E S. 1990. A unique neural timing system prevents male mice from harming their own offspring. Anita. Behav., 39: 535-539. PETRIE, M. 1994. Improved growth and survival of offspring of peacocks with more elaborate trains. Nature, 371: 598-599. PROMISLOW, D. E. L.; SMITH, E. A.; PEARSE, L. 1998. Adult fitness consequences of sexual selection in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA, 95: 10687-10692. PUSEY, A.; WILLIAMS,J.; GOODALL,J. 1997. The influence of dominance rank on the reproductive success of female chimpanzees. Science, 277: 828-831. QVARNSTR()M, A.; FORSGREN,E. 1998. Should females prefer dominant males? Trends Ecol. Evol., 13: 498-501. REYNOLDS,J. D.; GROSS,M. R. 1992. Female mate preference enhances offspring growth and reproduction in a fish, Poecilia reticulata. Proc. R. Soc. Lond. B, 250: 57-62. ROLDAN, E. R. S.; CASSINELLO,J.; ABAIGAR,Z.; GOMENDIO,M. 1998. Inbreeding, l]uctuating asymmetry, and ejaculate quality in an endangered ungulate. Proc. R. Soc. Lond. B, 265: 243-248. ROLDAN,E. R. S.; GOMENDIO,M. 1995. Sperm length and sperm competition in primates: a rebuttal of criticism. Folia Primatol., 64: 225-230. RYAN, M. J.; WAGNER,W. E. 1987. Asymmetries in mating preferences between species: female swordtails prefer heterospecific males. Science, 236: 595-597. RYAN, M. J.; FOX, J. H.; WILCZYNSKI,W.; RAND, A. S. 1990. Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature, 343: 66-67. SCHWAGMEYER,P. L.; PARKER,G. A. 1990. Male mate choice as predicted by sperm competition in thirteenlined ground squirrels. Nature, 348: 62-64. SILLEN-TULLBERG,B.; MOLLER, A. P. 1993. The relationship between concealed ovulation and mating systems in anthropoid primates: a phylogenetic analysis. Amer. Naturalist, 141 : 1-25. SMALL, M. E 1989. Female choice in nonhuman primates. Yrbk. Phys. Anthropol., 32: 103-127.

16

R.R. STALLMANNt~ J. W. FROEHLICH

SMUTS, B. B. 1985. Sex and Friendship in Baboons. Aldine, Chicago. SMUTS,B. B. 1987a. Sexual competition and mate choice. In: Primate Societies, SMUTS,B. B.; CHENEV,D. L.; SEYFARTH,R. M.; WRANGHAM,R. W.; STRUHSAKER,T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 385-399. SMUTS, B. B. 1987b. Gender, aggression, and influence. In: Primate Societies, SMUTS,B. B.; CHENEY,D. L.; SEYFARTH,R. M.; WRANGHAM,R. W.; STRUHSAKER,T. Z. (eds.), Univ. of Chicago Press, Chicago, pp. 400-412. THIERRY, B.; AU]ARD,E; HODGES,J. K. 1996a. Correlations between behavioral, hormonal and morphological variations in the menstrual cycle of female Tonkean macaques. Paper presented at the International Primatological Society, American Society of Primatologists Joint Congress, Madison, Wisconsin. THIERRY, l . ; HEISTERMANN,M.; AUJARD,E; HODGES,J. K. 1996b. Long-term data on basic reproductive parameters and evaluation of endocrine, morphological, and behavioral measures for monitoring reproductive status in a group of semifree-ranging Tonkean macaques (Macaca tonkeana). Amer. J. Primatol., 39: 47-62. VANSCHAIK,C. P. 1983. Why are diurnal primates living in groups? Behaviour, 87: 120-144. VANVOORHIES,W. A. 1992. Production of sperm reduces nematode lifespan. Nature, 360: 456-458. WATSON,E J. 1990. Femaleenhanced male competition determines the first mate and principle sire in the spider Linyphia litigiosa (Lyniphiidae). Behav. Ecol. Sociobiol., 26: 77-90. WATSON,E J. 1998. Multi-male mating and female choice increases offspring growth in the spider Neriene litigiosa (Linyphiidae). Anita. Behav., 55: 387-403. WHI'VrEN, P. L., RUSSELL,E. 1996. Information content of sexual swellings and fecal steroids in sooty mangabeys ( Cercocebus torquatus atys). Amer. J. Primatol., 40: 67-82. WICKLER,W. 1967. Socio-sexual signals and their intra-specific imitation among primates, ln: Primate Ethology, MORRIS,D. (ed.), Doubleday, New York, pp. 89-189. WILDT, D. E.; DOYLE, L. L.; STONE, S. C.; HARRISON,R. M. 1977. Correlation of perineal swelling with serum ovarian hormone levels, vaginal cytology, and ovarian follicular development during the baboon reproductive cycle. Primates, 18:261-270. WILSON, N.; TUBMAN,S. C.; LADY,P. E.; ROBERTSON,G. W. 1997. Female genotype affects male success in sperm competition. Proc. R. Soc. Lond. B, 264: 1491-1495. WOODROFFE,R.; VINCENT,A. 1994. Mother's little helpers: patterns of male care in mammals. Trends Ecol. Evol., 9: 294-297. WRANGHAM,R. W. 1993. The evolution of sexuality in chimpanzees and bonobos. Human Nature, 4: 47-79. YASUI, Y. 1997. A "good-sperm" model can explain the evolution of costly multiple matings by females. Amer. Naturalist, 149: 573-584. ZAHAVl,A. 1975. Mate selection: a selection for a handicap. J. Theor. Biol., 53: 205-214. ZEH, J. A. 1997. Polyandry and enhanced reproductive success in the harlequin-beetle-riding pseudoscorpion. Behav. Ecol. Sociobiol., 40:111 - 118. ZUMPE, D.; MICHAEL,R. P. 1987. Relation between the dominance rank of female rhesus monkeys and their access to males. Amer. J. Primatol., 13: 155-169. ZUMPE, D.; MICHAEL,R. P. 1989. Female dominance rank and behavior during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta). Amer. J. Primatol., 17: 287-304.

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Received: July 31, 1998; Accepted: August 26, 1999

Authors' Names and Present Addresses: ROBERTR. STALLMANN,Department of Anthropology, University afCal(fornia, Davis, California 95616. U. S. A. e-mail:[email protected];JEFFERYW. FROEHLICH.Department of Anthropology. University of New Mexico, Albuquerque. New Mexico 87131, U. S. A. e-mail:[email protected]