Female calls in lek-mating birds: indirect mate choice, female competition for mates, or direct mate choice?

I tested predictions from ultimate hypotheses of why femalegreat snipe Gallinago media give loud calls when visiting leks,using observational data and playback experiments. One hypothesisis that calls might be used in female—female competitionfor popular males, either (1) in an aggressive context towarda specific female, or (2) toward females in general to defendthe male. It has also been suggested that female calls (3) may not have an adaptive function, the capability of vocalizingbeing explained as a correlated response to selection on malesinging. Further, calls might function as (4) a copulationsolicitation toward a specific male. Finally, calls might havea function in mate choice, either (5) in indirect mate choiceas a fertility advertisement to incite male fighting, or (6)in direct mate choice as a mate-sampling aid to provoke quality-revealing responses from males. Disproportionately many female calls wereuttered when no other females were present on a male's territoryand in territories of males without mating success, contradictinghypotheses 1 and 2. Female calls were not associated with copulation;calls generally occurred several days before copulations, contradictinghypotheses 4 and 5. Playback of female calls attracted malesand increased fighting among males, even if females were presentnearby, contradicting hypothesis 3. Males changed their ownsongs in response to playback, and the response was relatedto their mating success. Taken together, the results are onlyconsistent with one of the hypotheses considered—femalecalls may function as a mate-sampling aid used in direct matechoice.     

How is female mate choice affected by male competition?

The plethora of studies devoted to the topics of male competition and female mate choice belie the fact that their interaction remains poorly understood. Indeed, on the question of whether competition should help or hinder the choice process, opinions scattered throughout the sexual selection literature seem unnecessarily polarised. We argue, in the light of recent theoretical and empirical advances, that the effect of competition on mate choice depends on whether it results in the choosy sex attaining high breeding value for total fitness, considering both direct and indirect fitness benefits. Specifically, trade-offs may occur between different fitness benefits if some are correlated with male competitive ability whilst others are not. Moreover, the costs and benefits of mating with competitive males may vary in time and/or space. These considerations highlight the importance of injecting a life-history perspective into sexual selection studies. Within this context, we turn to the sexual selection literature to try to offer insights into the circumstances when competition might be expected to have positive or negative implications for pre-copulatory female choice. In this regard, we elaborate on three stages where competition might impact upon the choice process: (i) during mate detection, (ii) mate evaluation, and (iii) in dictating actual mating outcomes. We conclude by offering researchers several potentially rewarding avenues for future research.     

Burrow ornamentation in the fiddler crab (Uca leptodactyla): female mate choice and male–male competition

Non-biological ornamentation is found in the nests and burrows of different kinds of animals. We evaluated here whether sand hoods constructed by male fiddler crabs (Uca leptodactyla) are one of the signals used by males to attract females during courtship. We observed females when they were walking among the males, and we quantified the proportion of females that visited male burrows with and without ornamentation and the choice to stay in a male’s burrow. Females visited more burrows with hoods than burrows without hoods, and they chose significantly more builder males. Male investment in ornamentation nevertheless decreased when the proportion of females increased in the area. Male investment was not correlated with the proportion of non-builder males nearby, but was positively correlated with overall density. The density sex ratio, however, was more male-biased in high-density than in low-density areas suggesting that even if building attracts females, the function could be related to male competition for mates.     

A colour and size dimorphism in the green swordtail (population Jalapa): female mate choice,male–male competition,and male mating strategies

Two types of males are present in the Jalapa population of Xiphophorus helleri: Males with a black or dark brownish mid-lateral stripe ("black males") mature earlier and are smaller than males with a red or brownish mid-lateral stripe ("red males"). We tested the hypothesis that the colour patterns of red males may be regarded as ornaments, which evolved as the result of inter- and/or intrasexual selection. As predicted, in choice tests females exhibited a strong preference for red versus black males. Furthermore, in competition experiments red males became dominant over black males with no exception, both when body size was equal and even when red males were 3–5 mm smaller than black males. However, contrary to our prediction, sneak–chase behaviour in black males was not detected, and courtship displays occurred at similar rates in both morphs. Red males are always heterozygous, with one allele for red and another for black colouration. This genetic constraint potentially prevents the extinction of the black morph. Possibly, the colour patterns of red males are functioning as indicators of heterozygosity. According to the "heterozygosity theory of mate choice", the female's preference for red males may be adaptive.     

Intraspecific mating system evolution and its effect on complex male secondary sexual traits: Does male–male competition increase selection on size or shape?

Sexual selection is generally held responsible for the exceptional diversity in secondary sexual traits in animals. Mating system evolution is therefore expected to profoundly affect the covariation between secondary sexual traits and mating success. Whereas there is such evidence at the interspecific level, data within species remain scarce. We here investigate sexual selection acting on the exaggerated male fore femur and the male wing in the common and widespread dung flies Sepsis punctum and S. neocynipsea (Diptera: Sepsidae). Both species exhibit intraspecific differences in mating systems and variation in sexual size dimorphism (SSD) across continents that correlates with the extent of male–male competition. We predicted that populations subject to increased male–male competition will experience stronger directional selection on the sexually dimorphic male foreleg. Our results suggest that fore femur size, width and shape were indeed positively associated with mating success in populations with male‐biased SSD in both species, which was not evident in conspecific populations with female‐biased SSD. However, this was also the case for wing size and shape, a trait often assumed to be primarily under natural selection. After correcting for selection on overall body size by accounting for allometric scaling, we found little evidence for independent selection on any of these size or shape traits in legs or wings, irrespective of the mating system. Sexual dimorphism and (foreleg) trait exaggeration is therefore unlikely to be driven by direct precopulatory sexual selection, but more so by selection on overall size or possibly selection on allometric scaling.     

Female–female competition or male mate choice? Patterns of courtship and breeding behavior among feral horses (Equus caballus) on Assateague Island

Previous research on the Assateague horses found that high-ranking females had more surviving offspring than low-ranking females. Variance in reproductive success may be the result of a variety of proximate processes that affect sexual behavior such as mate choice and mate competition. A study was done to determine whether patterns of courtship, social, and sexual behavior could be identified that would suggest mate choice and/or mate competition. Behavioral data were collected from approximately 40 sexually mature mares living in harem bands. Stallions showed more interest in the eliminations of dominant mares than subordinate mares. Males also engaged in significantly more high-intensity (e.g., mounts and copulations) sexual behavior with dominant mares than subordinate mares, and there was a trend for males to engage in more low-intensity (e.g., flehmen and ano-genital sniffing) sexual behavior with dominant mares than subordinate mares. There was no effect of mare rank on spatial relationships with the stallion; however, dominant mares did attempt to restrict reproductive access to the stallion by harassing and disrupting copulations. Higher foaling rates among dominant mares on Assateague Island could therefore be the result of rank-related mate choice by stallions and direct female competition for mating opportunities.     

Inbreeding avoidance in rhesus macaques: Whose choice?

Whether nonhuman primates avoid copulating with close kin living in their social group is controversial. If sexual aversion to relatives occurs, it should be stronger in females than in males because of females' greater investment in each offspring and hence greater costs resulting from less viable offspring. Data presented here show that adult male rhesus macaques breeding in their natal groups at Cayo Santiago experienced high copulatory success, but copulated less with females of their own matrilineages than with females of other matrilineages. Adult females were never observed to copulate with males of their own matrilineage during their fertile periods. Although natal males sometimes courted their relatives, examination of two measures of female mate choice showed that females chose unrelated natal males over male kin. Female aversion to male kin was specific to the sexual context; during the birth season, females did not discriminate against their male relatives in distributing grooming. Evolved inbreeding avoidance mechanisms probably produce different outcomes at Cayo Santiago than in wild rhesus macaque populations. Gender differences in sexual aversion to relatives may be partly responsible for differences between studies in reported frequency of copulations by related pairs. © 1993 Wiley-Liss, Inc.     

Male–male competition facilitates female choice in sticklebacks

In many species, secondary sexual characteristics are used in both male–male competition and in attracting females. This suggests that social control of deception could contribute to the maintenance of honest sexual signalling. In the three-spined stickleback Gasterosteus aculeatus, male red breeding coloration plays a dual role in sexual selection by functioning as both a threat signal in male–male competition and as a cue for female choice. To investigate whether male competition determines the level of signalling, the expression of red coloration and courtship activity were recorded both before and after male interactions. The results show that male competition influences signal expression by increasing the difference between males in signalling level. This in turn facilitates female choice and induces a preference for dominant males. Since a preference for dominant males may benefit females both directly and indirectly in this species with exclusively paternal care, male–male competition seems to increase the honesty of signalling and, thus, facilitates female choice in relation to male quality. This may increase the intensity of sexual selection and promote the evolution of breeding aggregations.     

Female mate preference in goby Eviota prasina: do secondary sexual traits influence female choice?

Males of the small gobiid fish Eviota prasina have longer dorsal fins than females and use their dorsal fins for courtship displays and male-male competition. We examined the influence of male dorsal fin length as well as the frequency of courtship displays on female mate preference using sequential choice experiments. Females responded more frequently to courting males with longer dorsal fins than males with shorter dorsal fins. This indicates female mate preference on the basis of male dorsal fin length in this goby. In addition, the logistic regression analysis showed that male courtship frequency positively influenced female mate preference. Since males incur costs to produce and maintain longer dorsal fins and to perform frequent courtship displays, these secondary sexual traits may indicate the quality of physical characteristics. In E. prasina, only males conducted parental care for eggs in their nests. Therefore, females may be able to ensure greater survival rates as well as higher genetic quality of their offspring by choosing males with better qualities based on these male traits.     

Female macaques compete for ‘power’ and ‘commitment’ in their male partners

The formation of male-female social bonds and the resulting competition among females for male partners is a core element of human societies. While female competition for a male partner outside the mating context is well studied in humans, evidence from non-human primates is scarce, and its evolutionary roots remain to be explored. We studied two multi male – multi female groups of wild Assamese macaques (Macaca assamensis), a species where females gain benefits from selectively affiliating with particular males. Using a behavioral data set collected over several years, we tested whether females competed over access to male social partners, whether success in competition was driven by female dominance rank, and which male traits were most attractive for females. We found assortative bonding by dominance rank between females and males, which together with females initiating and maintaining contact suggests direct female competition over males. Two male traits independently predicted male attractiveness to females: (1) current dominance rank, a measure of 'power' or a male's ability to provide access to resources, and (2) prior male affiliation with immatures, a measure of a male's potential paternal proclivity or 'commitment' to infant care. Both traits have been consistently identified as drivers of female partner choice in humans. Our study adds to the evidence that female competition for valuable male partners is not unique to humans, suggesting deep evolutionary origins of women's mate choice tendencies for ‘power’ and ‘commitment’.     

Does divergence in female mate choice affect male size distributions in two cave fish populations?

Sexual selection by female choice can maintain male traits that are counter selected by natural selection. Alteration of the potential for sexual selection can thus lead to shifts in the expression of male traits. We investigated female mate choice for large male body size in a fish (Poecilia mexicana) that, besides surface streams, also inhabits two caves. All four populations investigated, exhibited an ancestral visual preference for large males. However, only one of the cave populations also expressed this female preference in darkness. Hence, the lack of expression of female preference in darkness in the other cave population leads to relaxation of sexual selection for large male body size. While P. mexicana populations with size-specific female mate choice are characterized by a pronounced male size variation, the absence of female choice in one cave coincides with the absence of large bodied males in that population. Our results suggest that population differences in the potential for sexual selection may affect male trait variation.     

Female mate choice and the potential for ornament evolution in túngara frogs Physalaemus pustulosus

The potential for ornament evolution in response to sexual selection rests on the interaction between the permissive-ness or selectivity of female preferences and the constraints on male development of signaling related traits. We investigate the former by determining how latent female preferences either exaggerate the magnitude of current traits (I.e. Elaborations) or favor novel traits (I.e. Innovations). In tungara frogs, females prefer complex mating calls (whine-chucks) to simple calls (whine only). The whine is critical for mate recognition while the chuck further enhances the attractiveness of the call. Here we use a combina-tion of synthetic and natural stimuli to examine latent female preferences. Our results show that a diversity of stimuli, including conspecific and heterospecific calls as well as predator-produced and human-made sounds, increase the attractiveness of a call when added to a whine. These stimuli do not make simple calls more attractive than a whine-chuck, however. In rare cases we found stimuli that added to the whine decrease the attractiveness of the call. Overall, females show strong preferences for both elaborations and innovations of the chuck. We argue that the emancipation of these acoustic adornments from mate recognition allows such female permissiveness, and that male constraints on signal evolution are probably more important in explaining why males evolved their specific adornment. Experimentally probing latent female preferences for stimuli out of the species' range is a useful means to gain insights about the potential of female choice to influence signal evolution and thus the astounding diversity in male sexually-selected traits.     

Why do multiple traits determine mating success? Differential use in female choice and male competition in a water boatman

Mating success is often determined by multiple traits, but why this occurs is largely unknown. Much attention has been paid to female preferences for multiple traits, but surprisingly few researchers have addressed the possibility that multiple traits are important because they serve different functions in female choice and male-male competition. Differential trait function could result from a conflict of interest between the sexes or from constraints forcing the sexes to pay attention to different traits. I show that traits determined at distinct life-history stages differ in their importance in female choice and male-male competition in a water boatman Sigara falleni. Juvenile conditions determined body and foreleg pala size and were the main determinants of mating success under female choice, whereas adult conditions determined body mass and influenced mating success when male competition was included. This differential use of condition-dependent traits under the two selection regimes appeared to arise partly from a conflict between the sexes, since the two selection forces (female choice and male competition) conflict for selection on pala size, and partly from constraints, as females appeared unable to assess adult condition.     

Does sexual experience affect the strength of male mate choice for high‐quality females in Drosophila melanogaster?

Although females are traditionally thought of as the choosy sex, there is increasing evidence in many species that males will preferentially court or mate with certain females over others when given a choice. In the fruit fly, Drosophila melanogaster, males discriminate between potential mating partners based on a number of female traits, including species, mating history, age, and condition. Interestingly, many of these male preferences are affected by the male''s previous sexual experiences, such that males increase courtship toward types of females that they have previously mated with and decrease courtship toward types of females that have previously rejected them. D. melanogaster males also show courtship and mating preferences for larger females over smaller females, likely because larger females have higher fecundity. It is unknown, however, whether this preference shows behavioral plasticity based on the male''s sexual history as we see for other male preferences. Here, we manipulate the sexual experience of D. melanogaster males and test whether this manipulation has any effect on the strength of male mate choice for large females. We find that sexually inexperienced males have a robust courtship preference for large females that is unaffected by previous experience mating with, or being rejected by, females of differing sizes. Given that female body size is one of the most common targets of male mate choice across insect species, our experiments with D. melanogaster may provide insight into how these preferences develop and evolve.     

Divergence in mate choice systems: does evolution play by rules?

Understanding the genetic bases of phenotypes associated with the earliest stages of divergence will reveal a great deal about species formation. I review a number of model systems, most involving plant–insect interactions, that have already revealed genetic aspects of incipient speciation. It is suggested that progress in understanding the causal forces driving mating signal evolution and incipient speciation will be expedited in model systems where; (1) ecological and evolutionary information is available, (2) different aspects of mating behaviors that function in mate and/or species recognition are known, (3) genetic analysis of single phenotypes is undertaken, (4) analysis of sexual selection and isolation is performed under natural conditions (or in the wild), and (5) comparative data from related species are available to assess phylogenetic trends.     

Do males choose their mates in the lekking moth Achroia grisella? Influence of female body mass and male reproductive status on male mate choice

Lekking males aggregate to attract females and contribute solely to egg fertilization, without any further parental care. Evolutionary theory therefore predicts them to be nonchoosy toward their mates, because any lost mating opportunities would outweigh the benefits associated with such preferences. Nevertheless, due to time costs, the production of energetically costly sexual displays, and potential sperm limitation, the mating effort of lekking males is often considerable. These factors, combined with the fact that many females of varying quality are likely to visit leks, could favor the evolution of male mate preferences. Here, we show that males of the lekking lesser wax moth, Achroia grisella, were indeed more likely to mate with heavier females in choice experiments, even at their virgin mating (i.e., when their reproductive resources have not yet been depleted by previous matings). This differential female mating success could not be attributed to female behavior as heavy and light females showed similar motivation to mate (i.e., latency to approach the males) and time to copulate. Males seem to benefit from mating with heavier females, as fecundity positively correlated with female mass. This new empirical evidence shows that male mate choice may have been underestimated in lekking species.     

Sexual selection and sperm competition in primates: What are male genitalia good for?

One hundred twenty-five years ago, in The Descent of Man and Selection in Relation to Sex,¹ Charles Darwin proposed the theory of sexual selection, as distinct from natural selection, to explain why, in some species, males have such magnificent ornaments and, in other species, such impressive weapons. He suggested two processes, which we now term female choice and male-male competition: either females choose particularly ornate males or, alternatively, relatively passive females accept the winner of fights among males. By now, knowledge of species in which the females are more brightly colored or aggressive than males has led to a more general formulation of the principle of sexual selection, in which, instead of “females”, we write “the sex with the lower potential reproductive rate”, and, instead of “male”, “the sex with the higher potential reproductive rate”.²