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     

Size of sexual swellings reflects ovarian function in chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>)

While many theories exist on the evolution of the sexual swelling signal in female primates, the significance of the very large and variable swellings found in some catarrhine primates is still debated. As suggested by Pagel [(1994) Anim Behav 47:1333–1341], these exaggerated and costly signals have the potential to provide information about differential female reproductive quality to males. While Domb [(2000) Department of Anthropology, Harvard University, Cambridge] and Domb and Pagel [(2001) Nature 410:204–206] propose that swellings serve to reliably indicate between-female fitness differences, we hypothesize that they may indicate current reproductive cycle quality, within or between females. This study examines the between-cycle relationship between ovarian function, gauged via fecal steroid analysis, and absolute size of sexual swellings, yielded through photogrammetric methods. Fourteen cycles from eight captive, group-living chimpanzees (Pan troglodytes) exhibited considerable variability both in ovarian steroid levels and maximum sexual swelling size. Nearly all measures of a female's maximal swelling in a cycle correlated with early follicular and early luteal estradiol averages and the duration of luteal progesterone elevation. Swelling area was also correlated with late follicular estradiol. Given past evidence that such measures of ovarian function predict conceptive success, these data strongly suggest that swellings could convey information to competing males about the fecundability of a potential mate.Communicated by C. Nunn     

Sperm competition promotes diversity of sperm bundles in <Emphasis Type="Italic">Ohomopterus</Emphasis> ground beetles

Diversification of sperm morphology has been investigated in the context of sperm competition, but the adaptive significance of sperm bundles is still unclear. In analyzing 10 taxa of the genus Carabus subgenus Ohomopterus and one related Carabus ground beetles, we found that dimorphic sperm bundles occurred in most species with varied degrees of bimodality, whereas sperm were generally monomorphic. Comparative analyses with phylogenetically independent contrasts revealed that the sizes of large and small sperm bundles evolved more rapidly than, and were not correlated with, the length of sperm, suggesting more intense selection on sperm bundle sizes and their independent responses to different evolutionary forces. The size of large sperm bundles was positively correlated with male genital morphology (pertinent to displacement of rival spermatophores) and postcopulatory guarding duration as well as male body length, suggesting that larger sperm bundles have been favored when the risk of spermatophore displacement is high. Larger sperm bundles may be advantageous because of their ability to migrate more rapidly into the spermatheca. In contrast, no clear association was detected between the small sperm bundle size and mating traits despite its rapid diversification. The present study provides the first record of heteromorphic sperm bundles, the diversity of which may be promoted by sperm competition.     

The attractiveness fragment—AFLP analysis of local adaptation and sexual selection in a caeliferan grasshopper, <Emphasis Type="Italic">Chorthippus biguttulus</Emphasis>

Genetic variability among males is a necessary precondition for the evolution of female choice based on indirect genetic benefits. In addition to mutations and host–parasite cycles, migration of locally adapted individuals offers an explanation for the maintenance of genetic variability. In a previous study, conducting a reciprocal transplant experiment on a grasshopper, Chorthippus biguttulus, we found that environmental conditions significantly influenced not only body condition but also an important trait of male calling song, the amplitude of song. Although not significant, all other analysed physical and courtship song traits and attractiveness were superior in native than in transferred males. Thus, we concluded that local adaptation has a slight but consistent influence on a range of traits in our study populations, including male acoustic attractiveness. In our present study, we scanned male grasshoppers from the same two populations for amplification fragment length polymorphism (AFLP) loci connected with acoustic attractiveness to conspecific females. We found greater differences in allele frequencies between the two populations, for some loci, than are expected from a balance between drift and gene flow. These loci are potentially connected with locally adapted traits. We examined whether these alleles show the proposed genotype environment interaction by having different associations with attractiveness in the two populations. One locus was significantly related to sexual attractiveness; however, this was independent of the males’ population affiliation. Future research on the evolution of female choice will benefit from knowledge of the underlying genetic architecture of male traits under intraspecific sexual selection, and the ‘population genomics’ approach can be a powerful tool for revealing this structure.     

Postcopulatory sexual selection favours intrinsically good sperm competitors

We used guppies to study repeatability in sperm competitiveness and postcopulatory sexual selection on male ornamentation. In a block design involving 25 pairs of males, artificial insemination was used to mate each pair (A and B) to four unrelated females—two that were mated with the combined ejaculates of both males (sperm-competition treatment) and two receiving sperm from each of the two males individually (single-male treatment). Our analysis revealed significantly repeatable patterns of paternity across females in the sperm-competition treatment, suggesting that certain males are intrinsically better sperm competitors than others, irrespective of female identity. Next, we compared mean brood success (number of offspring per brood) between sperm competition and single-male treatments. We found no significant effect of treatment on female fecundity, suggesting that the previously reported direct benefits of polyandry in this species may be due to factors such as differential maternal effects or differences in the number of inseminated sperm between treatments. Our artificial insemination assay was designed to control both factors. Finally, we determined whether variation in relative paternity was random with respect to male phenotype. Unlike previous work on Trinidadian populations, we found no significant relationship between male sexual ornamentation and sperm competitiveness in the focal population.     

Sperm removal and ejaculate size correlate with chelae asymmetry in a freshwater crayfish species

Asymmetry in traits of sexual relevance may impair copulation behaviour and sexual performance of males, ultimately resulting in a fitness cost. Freshwater crayfish males use chelae, a sexually selected trait, to secure and position the female prior to and during mating. Thus, a relatively large chelae asymmetry, resulting from accidental loss and regeneration of one cheliped after autotomy, could have great consequences for male sexual behaviour. We studied copulatory behaviour and sperm expenditure of males paired to a mated female in Austropotamobius italicus, a freshwater crayfish species where both male and female mate multiply and where last-mating males are able to actively remove previously deposited sperm. We aimed at assessing whether male sperm removal and expenditure varied according to sperm allocated by first-mating males, and according to copulation behaviour and phenotypic traits (carapace length, chelae length and relative chelae asymmetry) of second-mating males. Second-mating males did not adjust their ejaculate size in relation to first-mating male ejaculate, nor to the first-mating male’s sperm removed. Moreover, the amount of sperm removed by second-mating males increased with increasing first-mating males ejaculate size, and first-mating male sperm remaining after removal did not correlate with the original first-mating male ejaculate size. Interestingly, the amount of sperm removed by second-mating males decreased with increasing relative chelae asymmetry, while increasing with male body size. However, second-mating (but not first-mating) asymmetric-clawed males produced larger ejaculates than symmetric-clawed ones. Importantly, the proportion of second-mating male sperm remaining after the two matings did not vary with relative chelae asymmetry nor with body size of second-mating males. Thus, small, asymmetric-clawed crayfish males appear to adopt sperm allocation tactics that allow them to fully compensate for their inferior sperm removal ability.     

Extrapair paternity in the swamp sparrow, <Emphasis Type="Italic">Melospiza georgiana</Emphasis>: male access or female preference?

Over the past two decades, the combination of molecular and field methods has revealed considerable variation in the level of extrapair fertilizations among socially monogamous birds. Models predicting extrapair young range in scale from a single population to multiple Orders, and there is no single, unifying theory for these reproductive tactics. We investigated proximate explanations of extrapair fertilizations in two subspecies of the swamp sparrow, Melospiza georgiana georgiana and Melospiza georgiana nigrescens, across a range of social and environmental conditions. The presence of extrapair young was best predicted by the size of two male plumage badges (one correlated with parental care and one with territorial aggression) relative to the badge size of their immediate neighbors, the interaction of these two measures, mean territory size, and the maximum size of the aggression badge among neighbors. The size of the male’s parental care badge (relative to neighbors) was negatively correlated with the probability of lost paternity. The relative size of the aggression badge was positively correlated with the presence of extrapair young when the parental care badge was small and negatively correlated when the badge was large. Controlling for these crown measures, males with larger territories were less likely to suffer losses in paternity. There was no effect of breeding density, breeding synchrony, their interaction, subspecies, or weather during the fertile period on the presence of extrapair young. These results suggest that female preference for males that provide more parental care (or preference for genes that convey this trait) plays a dominant role in extrapair interactions among swamp sparrows. Models based on female assessments of relative mate quality offer a promising explanation of patterns in extrapair fertilizations among bird species.     

Influence of male harassment and female competition on female feeding behaviour in a sexual–asexual mating complex of mollies (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>, <Emphasis Type="Italic">P. formosa</Emphasis>)

Differential interests between the sexes regarding the number of copulations can result in sexual harassment. Hence, females may have less time available for foraging. Male sexual harassment often leads to fitness reduction in females. We used the mating complex of the bisexual fish Poecilia mexicana and the co-occurring all-female Poecilia formosa to study sexual harassment and its incurred cost on female feeding efficiency. P. formosa is a sperm-dependent parthenogen that requires mating with host males to induce embryogenesis, but the male genes are not used. We therefore predicted P. mexicana males to prefer conspecific females. Hence, costs of male sexual harassment should not occur in unisexuals. While P. formosa are at a disadvantage compared to P. mexicana females due to male mate choice (leading to sperm limitation), this could be traded-off by suffering less from sexual harassment. In our experiment, we found males to direct significantly more pre-copulatory mating behaviour towards conspecific females, whereas actual mating attempts did not differ between species. Contrary to our prediction, both types of females started feeding later and spent less time feeding in the presence of a male partner compared to the time spent feeding with another female, suggesting that females of both species suffer from male harassment. The focal females' feeding time declined with increasing body size of the female competitor, and the same pattern was found when a male was present. We discuss that—besides sexual harassment—other factors such as food competition and female mate choice may affect female feeding efficiency.     

Lack of innate preference for morph and species identity in mate-searching <Emphasis Type="Italic">Enallagma</Emphasis> damselflies

Insect mate recognition is often viewed as stereotypic, innate, and species-specific. However, male damselflies can learn to identify female-specific color morphs as potential mates. A suite of male mimicry hypotheses assume that heteromorphic females, which differ from males in color pattern, are more easily recognized as “female” and thus lack the inherent, anti-harassment advantage that the more male-like signal provides for andromorphs. Using two measures of male preference, we investigated whether naïve males have a preexisting sensory bias for a given morph color in Enallagma civile, a species that appeared to exhibit extreme plasticity in morph expression across generations within a breeding season. E. civile males raised in the absence of females exhibited no preference for either morph, whereas males raised with one female type exhibited a learned sensory bias for that morph. Male Enallagma also lacked a bias toward conspecific females over a congeneric sister species. In a naturally naïve population of Enallagma ebrium, males reacted sexually to both morphs of Enallagma hageni as often as they did to conspecific females, whose thoracic spectra were nearly identical with those of E. hageni. Moreover, despite the similar thoracic spectra of males and andromorphs, both of which reflected UV, males rarely reacted sexually to other males. Our results falsified implicit assumptions of male mimicry hypotheses, supported learned mate recognition, and suggested a scenario for speciation via sexual conflict.