The efficacy of female choice in chimpanzees of the Taï Forest, Côte d’Ivoire

Male–male competition has historically been considered the major force driving sexual selection. However, female choice and inter-sexual conflict are increasingly recognized as important influences affecting differential mating and reproductive success. Many females exhibit preferences for particular males; however, male strategies may conflict with females’ ability to obtain their mate preferences. To influence paternity, females must affect both (1) whether or not sexual interactions occur, particularly during the periovulatory period (POP) and (2) the outcome of sexual interactions. This study focuses on the effectiveness of female choice in wild chimpanzees (Pan troglodytes verus). Over 2,600 h of data were collected on two habituated chimpanzee communities in the Taï National Park, Côte d’Ivoire. Female mate preferences were measured by quantifying proceptive and resistance behavior toward males in both the periovulatory period and non-POP phases of estrus. The efficacy of female preference was measured both (1) by measuring success rates of female proceptivity and resistance behaviors and (2) by determining how well measures of female mate preference (proceptivity and resistance rates) predict male mating success. Though male chimpanzees are clearly dominant to females, the results indicate that females could effectively resist male solicitations and, in most cases, unwanted copulations were averted. Both female proceptivity and resistance rates correlate (positively and inversely, respectively) with male mating success in POP. Outside POP, female proceptivity rates corresponded with male mating success, but resistance rates did not. Males (irrespective of rank) that were preferred by females obtained higher mating success compared to other males during the POP, suggesting that females were effective in their mate choice and that, despite clear male dominance, female choice influences paternity in wild chimpanzees.     

Vocalizations by Alaskan moose: female incitation of male aggression

Evidence of female fomentation of male–male aggression as a mechanism of mate choice is rare, especially in mammals. Female choice of mates in polygynous species may be masked by intense male competition or by males attempting to restrict female choice. We studied protest moans of female Alaskan moose Alces alces gigas in interior Alaska, USA, from 1987 to 1990, to determine if moans incited male–male aggression. Alaskan moose exhibit a mating system in which one dominant male (the harem master) herds, defends, courts, and attempts to mate with females in his harem. Protest moans were given by females only in response to courtship. We hypothesized that if protest moans were related to females reducing harassment and exercising mate choice, females should give protest moans more frequently when courted by small males and less often when courted by large males, and that rates of male–male aggression would be elevated following protest moans. Harems were composed of one large male, with a mean of 4.4 females (median = 3 females); 10% of 132 harems included ≥10 females. The temporal pattern of protest moans from late August through November was associated with, but tended to lag behind, mating behavior. The rate of protest moans given by females decreased with increasing size of males courting them. Male–male aggression was significantly less during periods without protest moans than during periods in which protest moans occurred. These results indicate that female moose gave protest moans to reduce harassment by smaller males, and assure a mating opportunity with the most dominant male. Such a subtle mechanism of indirect mate choice by females may occur in other vertebrates in which choice is limited by a mating system in which male–male combat and male dominance over females reduces opportunities for female choice. The importance of female choice may be undervalued in studies of sexual selection in mammals.     

Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda

Cooperative mate guarding by males is unusual in mammals and birds, largely because fertilizations are non-shareable. Chimpanzees live in fission-fusion communities that have cores of philopatric males who cooperate in inter-group aggression and in defending access to the females in their community. Male contest mating competition is restrained within communities, but single high-ranking males sometimes try to mate guard estrous females. Data from an unusually large chimpanzee commmunity at Ngogo, Kibale National Park, Uganda, that contains more males than any previously studied community show new variation in chimpanzee mate-guarding behavior. Contrary to expectation given the large number of males, mate guarding was as common as, or more common than, at other sites, and males other than the alpha male guarded more often. More strikingly, pairs or trios of top-ranking males sometimes engaged in cooperative aggression to prevent estrous females from mating with other males, but tolerated each other's mating activities. Both single males and coalitions mostly guarded periovulatory females. Mate-guarding coalitions were previously unknown in chimpanzees. Coalitions occurred in large mating parties, seemingly because these often contained too many males for single males to maintain exclusive access to estrous females. Coalition members gained higher shares of copulations than they could have expected from solo mate guarding, and suffered lower per capita costs of guarding (as inferred from aggression rates). Two males who most often participated in coalitions formed two-male coalitions at about the point where the number of males present made it unlikely that either could get 50% or more of total copulations on his own, and formed trios when this value dropped below 33%. Kin selection could be a factor in cooperation among male chimpanzees, but coalition members were not necessarily close relatives and the apparent structure of payoffs fit that of mutualism. Furthermore, reliance of male chimpanzees on support from allies to maintain high rank could have led to trading of mating exclusivity for support against mating competitors. Received: 28 May 1997 / Accepted after revision: 16 May 1998     

Repeatable female preferences, mating order and mating success in the poeciliid fish, Heterandria formosa

Sexual selection via female choice can afford preferred males comparably higher mating success than those males that lack preferred traits. In addition, many models of sexual selection assume that both male traits and female preferences are heritable. In this study we test whether females of the poeciliid fish, Heterandria formosa, have repeatable pre-copulatory preferences for larger males. We also test whether female pre-copulatory preferences are always reliable indicators of male mating success. When given a choice between a large and a small male, females prefer larger males, and the repeatability of this preference is high. Although there are no overall differences in male mating success between large and small males, large males have a higher mating success when they are the first to mate than when they are the second to mate. Likewise, preferred males also have higher mating success when they are the first to mate than when they mate second. Therefore, the repeatable female preferences observed in this study only predict male mating success when the preferred male mates first. These results illustrate that even significantly repeatable female preferences do not translate into male mating success, which is an assumption of many examinations of the importance of female choice in sexual selection.     

Does female aggression prevent polygyny? An experiment with pied flycatchers (Ficedula hypoleuca)

The female aggression hypothesis states that resident females may be able to prevent polygyny by behaving aggressively towards intruding females. A critical test of the hypothesis is to provide prospecting females with a choice between displaying mated males some of which have initial mates with artificially reduced levels of aggressiveness. Here we present a mate choice experiment on pied flycatchers Ficedula hypoleuca. The species is a cavity nester, and resident females were prevented from behaving aggressively by enclosing them within their own nestboxes: narrowing the entrance hole so that they could not escape but could still let their head out and have some contact with their mate. This treament had only a minor influence on male behaviour. We studied whether the experimental males were better able to attract a new female than a control group of mated males. Four predictions from the female aggression hypothesis were supported. (1) Mating success of control males was positively related to the distance between their primary and secondary territory. (2) For experimental males, mating success was unrelated to interterritorial distance. (3) Experimental males had higher mating success than control males when the interterritorial distance was short but (4) not when it was long. Experimental males had much lower mating success than unmated males, as would be expected if prospecting females are able to discover male mating status from cues other than visits by primary females to their mates' secondary nest sites. Received: 5 January 1998 / Accepted after revision: 30 December 1998     

Pre-copulatory sexual selection in the cigarette beetle Lasioderma serricorne

Traditional concepts of sexual selection and sexual conflict make different predictions about the costs and benefits to females of exposure to males with higher mating success. The traditional concepts of sexual selection assume that females benefit from their mate choices, whereas sexual conflict assumes that the females suffer greater costs by mating with males who have greater mating success and thus reduce their fitness. In order to understand how mate choice evolves, it is necessary to estimate the overall effect of mate choice on female fitness. However, relatively few studies have conducted that investigation. In this study, we investigated the direct and indirect effects of mating with attractive males on the fitness of females in the cigarette beetle Lasioderma serricorne. Mating with attractive males increased the number of female offspring but did not affect female longevity. Additionally, we found evidence that attractive males sire highly attractive sons. Thus, mating with an attractive male provides direct and indirect benefits but no fitness cost to female L. serricorne.     

Fighting success and attractiveness as predictors of male mating success in the black field cricket, Teleogryllus commodus: the effectiveness of no-choice tests

Females are generally assumed to prefer larger, more dominant males. However, a growing number of studies that control for male-male competition have shown no correlation between dominance and attractiveness. Aggressive males can interfere with female mate preference either by physically coercing females into mating or by driving submissive males away and restricting mate choice. The most common method of assessing female mate choice is by using simultaneous two-choice tests. These control for male-male interactions, but usually interfere with physical and chemical cues involved in mate selection or alter male behaviour. They are therefore unsuitable for many study species, especially insects. Another method is the no-choice test that measures a females latency to mating when placed with a single male as an indication of male attractiveness. No-choice tests control for male-male aggression while allowing full contact between pairs (they allow actual mating to be directly observed rather than to occur based on a correlated behaviour). So far, however, no study has confirmed that males that entice females to mate sooner actually enjoy increased longer-term mating success. As such, the accuracy of no-choice tests as a method of examining mate choice remains untested. Here, we used no-choice tests on the black field cricket, Teleogryllus commodus, to show that (1) females did not prefer males that won fights (dominant males), and (2) latency to mating predicts actual mating success. We have clearly demonstrated the usefulness of no-choice tests and, considering the advantages of this method, they should be more often considered for a wider variety of taxa.Communicated by D. Gwynne     

The assessment of female reproductive state during courtship and scramble competition in the fiddler crab, Uca paradussumieri

Male fiddler crabs, Uca paradussumieri, mate underground during a 4- to 7-day period each full and new moon. As soon as the tide recedes, males enter the burrows of females that will ovulate the following day ('pre-ovigerous' females). Males copulate with and guard these females until they ovulate. When interrupted by an intruding male, the first male to reach the female is usually able to defend her and successfully mate with her. In fiddler crabs, females mate multiply and there is last male sperm precedence. Before each semi-lunar mating period, male U. paradussumieri were more likely to court females with whom they would later mate than other nearby females with whom they did not mate. This suggests that males collect information on female reproductive state prior to the females becoming ovigerous. In this species, aggression was common between males that courted the same female. When previously courted females were approached by other males, the initial courter attempted to forcefully disrupt the courtship. This behavior may allow males the exclusive use of information on female reproductive condition. It also suggests a type of scramble competition between males over females. Furthermore, it indicates that males are able to locate receptive females prior to their becoming ovigerous. The shorter guarding period observed in this species, as compared with other fiddler crabs, is caused by females rejecting longer guarding periods. Male ability to assess female reproductive status may therefore be advantageous because it increases male mating success within a scramble type of competitive polygyny.     

Female tactics to reduce sexual harassment in the Sumatran orangutan (Pongo pygmaeus abelii)

Orangutan males demonstrate intrasexual dimorphism with corresponding alternative mating strategies. Sexual harassment is the predominant feature of the mating strategy that subadult males pursue. This study investigated the countertactics that females employ to reduce sexual harassment by subadult males. I observed 207 copulations during more than 9,000 h of focal follows of wild Sumatran orangutans at the Suaq Balimbing Research Station over a 23-month period. Rates of copulations initiated by subadult males increased during months of high fruit abundance, and most mating attempts were directed toward females with weaned infants. Simultaneous harassment by multiple subadult males increased significantly during months of high fruit abundance, and nearly all adult female-adult male consortships occurred during periods of high fruit abundance. Females who maintained spatial association with adult males, either via consortship or by nonmating temporary parties, received lower rates of harassment, as measured by the success rate of subadult male mating attempts. Adult female-adult male parties did not always result in mating between the associating dyad. Female initiation of protective services by adult males is one social tactic that female orangutans employ to reduce sexual harassment. Females therefore receive direct services from adult males, which may be one factor that influences female mate choice in Sumatran orangutans.     

Male mate choice favors more colorful females in the gift-giving cabbage butterfly

While the phenomenon of male mate choice has attracted considerable attention in the last two decades, whether this sexual selection mechanism could drive the evolution of female ornaments remains poorly understood. Here, we used experimental manipulation of female wing coloration to investigate male mate choice in Pieris rapae, a gift-giving butterfly. Further, we tested whether males’ nutritional status influenced their mating preferences by subjecting larvae to short periods of starvation. We found that males showed significantly more mating approaches toward control females with more colorful wings (higher pteridine content), and that this preference was strongest in low-nutrition males. Additionally, a study of field-collected females revealed that pteridine-based wing coloration was positively correlated with female egg load, which suggests such ornaments may signal female quality. Pteridine-based ornaments are widespread in nature, however their potential as honest signals in male mate choice remains largely unexplored. This work furthers our understanding of how male mate choice and female ornamentation may evolve in species whose mating systems include nutritional nuptial gifts.     

Phenotypic correlates and survival consequences of male mating success in lek-mating greater prairie-chickens (<Emphasis Type="Italic">Tympanuchus cupido</Emphasis>)

Female choice and male–male aggression are two modes of sexual selection that can lead to elaboration of male morphological and behavioral traits. In lek-mating species, male mating success is often strongly skewed, and it is puzzling why variation in male traits is still observed given directional female choice. If male traits correlated with reproductive success are honest signals of male quality, there may be survival costs associated with the expression of those traits. In this study, we examined whether morphological, behavioral, and territorial traits are correlated with male mating success and survival in the lek-mating greater prairie-chicken (Tympanuchus cupido). We introduce a novel application of multinomial discrete choice models for analysis of female mate choice behavior. We found that behavioral and territorial attributes showed 6.5 times more variability among males than morphological traits. Both display and aggressive behaviors were strong predictors of male mating success, suggesting that both female choice and male–male aggression were important in determining mating success among male greater prairie-chickens. Moreover, annual survival of male prairie-chickens was independent of mating success and male traits. Females appear to be choosing males based on behavioral traits where large variation exists between males (coefficient of variation >30%). Behavioral traits were the most important factor in determining mating success of male prairie-chickens, but the mechanism underlying this relationship is unknown. In the future, experimental manipulations of male hormones or parasite loads could bridge the proximate mechanisms and ultimate consequences of factors mediating male mating success in lek-mating grouse.     

Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d’Ivoire

According to sexual selection theory, females should selectively mate with high-quality males to enhance offspring survival and maximize reproductive success. Yet, chimpanzee (Pan troglodytes) females are known to mate promiscuously. Although there is substantial rationale for a promiscuous mating strategy, there is also a strong expectation that females should be selective, and the question arises as to whether promiscuity precludes female choice. The aims of this study are to: (1) compare wild female chimpanzee sexual strategies throughout estrus, and (2) determine whether females exhibit mate preferences for particular males. Over 2,600 h of data were collected on two habituated chimpanzee (Pan troglodytes verus) communities in the Taï National Park, Côte dIvoire. Female mate preferences were measured by quantifying proceptivity and receptivity toward males. Results indicate that all females exhibited proceptivity and resistance to male solicitations, but that there was substantial variation in their magnitudes within and among females. Female proceptivity rates were lower and resistance rates were higher in the periovulatory period (POP) when conception is most likely. Females were more selective during POP, and more promiscuous outside of POP, suggesting that females may follow a mixed reproductive strategy, being selective when conception is likely and more promiscuous when conception is unlikely. Results from this study emphasize the importance of considering the fertility window when determining female mate preferences, and of examining female behavior in POP and non-POP phases separately when evaluating hypotheses for multi-male mating.Communicated by C. Nunn     

Mate with the young, kill the old: reversed sexual cannibalism and male mate choice in the spider Micaria sociabilis (Araneae: Gnaphosidae)

Female mate choice is regarded as a strong selective force that significantly affects male mating success. In extreme cases, mate rejection can result in sexual cannibalism. However, males may choose between their partners as well. The killing of potential female mates, i.e. reversed form of sexual cannibalism, may be related to male mate choice. We examined male mate choice in the spider Micaria sociabilis, focusing on the roles of female mating status (virgin/mated), size and age. Reversed cannibalism reached its highest frequency in the period of generation overlap, i.e. when young males from the summer generation met old(er) females from the spring generation. These results suggest discrimination against old(er) females. The frequency of cannibalism was not affected by female mating status or female size. However, larger males from the summer generation were more cannibalistic than smaller males from the spring generation. We conclude that reversed sexual cannibalism might be an adaptive mate choice mechanism and can be explained in the context of the aggressive spillover hypothesis.     

Mating system and mating success of the desert spider Agelenopsis aperta

Field studies of the desert spider Agelenopsis aperta revealed a primarily monogamous mating system. However polygyny, polyandry and polygynandry were superimposed upon the primary system, with 9% of the marked males and 11% of the marked females in a field population mating more than once. In the laboratory males commonly mated multiply with fertile offspring resulting, while females were less likely than males to mate multiply. Monogamy under field conditions was enforced by two factors: (1) high travel costs to males, and (2) a significant decline in female receptivity after the first mating. Heavy males were more likely to be accepted by females both in the field, and in female choice experiments conducted in the laboratory. Finally, male weight determined the outcome of male-male agonistic interactions over females. One possible explanation for female choice in this system which lacks male parental investment is that females may be using male size as an indicator of future success of their offspring.     

Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus)

In a wide variety of species, male reproductive success is determined by contest for access to females. Among multi-male primate groups, however, factors in addition to male competitive ability may also influence paternity outcome, although their exact nature and force is still largely unclear. Here, we have investigated in a group of free-ranging Barbary macaques whether paternity is determined on the pre- or postcopulatory level and how male competitive ability and female direct mate choice during the female fertile phase are related to male reproductive success. Behavioural observations were combined with faecal hormone analysis for timing of the fertile phase (13 cycles, 8 females) and genetic paternity analysis (n = 12). During the fertile phase, complete monopolisation of females did not occur. Females were consorted for only 49% of observation time, and all females had ejaculatory copulations with several males. Thus, in all cases, paternity was determined on the postcopulatory level. More than 80% of infants were sired by high-ranking males, and this reproductive skew was related to both, male competitive ability and female direct mate choice as high-ranking males spent more time in consort with females than low-ranking males, and females solicited copulations mainly from dominant males. As most ejaculatory copulations were female-initiated, female direct mate choice appeared to have the highest impact on male reproductive success. However, female preference was not directly translated into paternity, as fathers were not preferred over non-fathers in terms of solicitation, consortship and mating behaviour. Collectively, our data show that in the Barbary macaque, both sexes significantly influence male mating success, but that sperm of several males generally compete within the female reproductive tract and that therefore paternity is determined by mechanisms operating at the postcopulatory level.     

Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (<Emphasis Type="Italic">Microcebus murinus</Emphasis>)

Sex-specific interests over the maximization of reproductive success lead to an inter-sexual conflict over the optimal mating system in a species. Traditionally, the outcome of this inter-sexual conflict has been studied from the male perspective but it also depends on female mating strategies, such as manipulating the temporal distribution of sexual activity, advertisement, and mate choice. We used a small nocturnal primate, the gray mouse lemur (Microcebus murinus) to determine the relative importance of female mating strategies on the outcome of this conflict in a species where females are solitary during their activity period. We studied their mating behavior over three consecutive annual mating seasons and determined the genetic relationships among more than 300 study animals to quantify individual reproductive success. We found that most females were receptive asynchronously. Females did not exhibit any obvious direct mate choice, probably due to a highly male-biased operational sex ratio and the corresponding costs of choosiness. However, females exercised indirect choice for multiple matings. They mated with 1–7 males up to 11 times during their single night of receptivity. As a result, mixed paternity was common but heavier males sired more offspring, meaning that indirect female choice for superior males cannot be excluded. Females exhibited a mixed mating strategy, avoiding costly direct mate choice but still counteracting male efforts to monopolize mating, successfully increasing genetic variability among offspring. Thus, females had a major influence on the outcome of the inter-sexual conflict despite male monopolization attempts.Communicated by J. Setchell     

Prior encounters with the opposite sex affect male and female mating behavior in a wolf spider (Araneae,Lycosidae)

Mate availability can vary widely in nature depending upon population density and sex ratio and can affect the ability of individuals to be selective in mate choice. We tested the effects of prior encounters with the opposite sex (i.e., exposure to the opposite sex either with or without mating) on subsequent mating behavior in two experiments that manipulated mate availability for both males and females in the wolf spider, Hogna helluo. The probability of mating in the experimental trial depended upon whether the prior encounter involved mating or not, and males and females responded in opposite directions. Exposure without mating resulted in a higher subsequent frequency of mating for females and a lower subsequent frequency of mating for males, while prior mating experience resulted in a lower frequency of female remating and a higher frequency of male remating. Prior exposure without mating did not affect female aggression. However, mated females engaged in precopulatory cannibalism more frequently than virgins. Mated males escaped postcopulatory cannibalism more frequently than virgins. Our results show that males respond to exposure without mating in the expected manner. However, prior mating (1 week earlier) had unexpected effects on males, which may be due to mated males being of higher quality. There were little or no effects of the size of the prior exposure individual or mate on subsequent mating behaviors. Further research is needed to determine why different species use different degrees of prior information in mate choice.     

Indirect fitness benefits are not related to male dominance in a killifish

Recent theoretical and empirical studies have shown that male dominance is often at odds with female mate preference and that indirect (genetic) benefits of mate choice may not be related to male dominance. We tested whether female preference corresponded to male dominance and whether mating with dominant males conveyed benefits to offspring fitness in a small freshwater fish, the African annual killifish Nothobranchius korthausae (Cyprinodontiformes), a species without parental care. The experimental design used controlled for the effect of male age, possibility of sperm and egg depletion, and accounted for a potential that females express their preference through maternal effects by manipulation of egg mass during ovulation. By sequentially mating females with males of known dominance, we found that female N. korthausae showed no mate preference in terms of egg numbers deposited with respect to male dominance or body size and no congruent mate preference to specific males was detected. However, males sired offspring with consistently higher hatching success and the effect was repeatable across individual females. Thus, some males provided females with indirect benefits related to additive genetic quality (“good genes”) and expressed via increased hatching rate, but this benefit was not related to male dominance status or body size.     

Sequential male mate choice in a fish,the Pacific blue-eye<Emphasis Type="Italic"> Pseudomugil signifer</Emphasis>

Mate choice is not just a female preoccupation. Under some circumstances, males may also be choosy. However, studies of male mate choice have generally been confined to situations where males can make direct comparisons between potential partners. In contrast, sequential male mate choice has largely been overlooked despite its biologically importance, especially if current investment in mate attraction diminishes a males future mating opportunities. Using the Pacific blue-eye fish Pseudomugil signifer, we show that males are capable of exercising sequential mate choice. When presented sequentially with large and small females, males spent more effort courting the former. However, males did not appear to modify the time spent courting a given female based on the size of the female encountered previously. We suggest that greater attention to the sequential choice problem in males may help illuminate similarities and differences between the sexes when it comes to mating decisions.Communicated by T. Czeschlik     

Time constraints and multiple choice criteria in the sampling behaviour and mate choice of the fiddler crab,Uca annulipes

Active female sampling occurs in the fiddler crab Uca annulipes. Females sample the burrows of several males before remaining to mate in the burrow of the chosen partner. Females time larval release to coincide with the following nocturnal spring tide and must therefore leave sufficient time for embryonic development after mating. Here we show how this temporal constraint on search time affects female choosiness. We found that, at the start of the sampling period (when time constraints are minimal), females selectively sample the larger males in the population. Towards the end of the sampling period (when the temporal constraints increase the costs of sampling), females are less selective. Furthermore, we suggest that the number of males sampled (and other indices of ‘‘sampling effort’’) may not be reliable indicators of female choosiness and may not reflect the strength of female mating preferences under certain conditions. Burrow quality also emerged as an important criterion in final mate choice. Burrow structure potentially influences reproductive success, and mate acceptance based on burrow structure appears to involve a relatively invariant threshold criterion. Since there is no relationship between male size and burrow quality, females are using at least two independent criteria when choosing potential mates. We envisage mate choice as a two-stage process. First, females select which males to sample based on male size. They then decide whether or not to mate with a male based on burrow features. This sampling process explains how two unrelated variables can both predict male mating success. Received: 23 March 1995/Accepted after revision: 14 January 1996