Polyandrous females avoid costs of inbreeding.

Why do females typically mate with more than one male? Female mating patterns have broad implications for sexual selection, speciation and conflicts of interest between the sexes, and yet they are poorly understood. Matings inevitably have costs, and for females, the benefits of taking more than one mate are rarely obvious. One possible explanation is that females gain benefits because they can avoid using sperm from genetically incompatible males, or invest less in the offspring of such males. It has been shown that mating with more than one male can increase offspring viability, but we present the first clear demonstration that this occurs because females with several mates avoid the negative effects of genetic incompatibility. We show that in crickets, the eggs of females that mate only with siblings have decreased hatching success. However, if females mate with both a sibling and a non-sibling they avoid altogether the low egg viability associated with sibling matings. If similar effects occur in other species, inbreeding avoidance may be important in understanding the prevalence of multiple mating.     

Females increase offspring heterozygosity and fitness through extra-pair matings

Females in a variety of species commonly mate with multiple males, and there is evidence that they benefit by producing offspring of higher genetic quality; however, the nature of these genetic benefits is debated. Enhanced offspring survival or quality can result from intrinsic effects of paternal genes---'good genes'--or from interactions between the maternal and paternal genomes--'compatible genes'. Evidence for the latter process is accumulating: matings between relatives lead to decreased reproductive success, and the individual level of inbreeding--measured as average heterozygosity--is a strong fitness predictor. Females should thus benefit from mating with genetically dissimilar males. In many birds, social monogamy restricts mate choice, but females may circumvent this by pursuing extra-pair copulations. Here we show that female blue tits, Parus caeruleus, increase the heterozygosity of their progeny through extra-pair matings. Females thereby produce offspring of higher reproductive value, because less inbred individuals have increased survival chances, a more elaborate male secondary sexual trait (crown colour) and higher reproductive success. The cost of inbreeding may therefore be an important factor driving the evolution of female extra-pair mating.     

Sexual selection for sensory exploitation in the frog Physalaemus pustulosus

The sensory bases of species and population mate preferences are well known; in frogs properties of the female auditory system influence such preferences. By contrast, there is little understanding of how sensory characteristics could result in sexual selection within a population. One possible mechanism is that females are more sensitive to male courtship signals that deviate from the population mean. We document this mechanism in the frog Physalaemus pustulosus. Female basilar papilla tuning is biased toward lower-than-average frequencies in the 'chuck' portion of the male's call, explaining female preference for the lower-frequency chucks produced by larger males. The tuning does not differ between P. pustulosus and its close relative P. coloradorum, a species in which males never evolved the ability to produce chucks; thus the female tuning evolved before the chuck and therefore the chuck played no role in the evolution of the preference. This allows us to reject two popular hypotheses for the evolution of this female preference (runaway sexual selection and natural selection) in favour of a third: sexual selection for sensory exploitation.     

Variable female preferences drive complex male displays

Complexity in male sexual displays is widely appreciated but diversity in female mate choice has received little attention. Males of many species have sexual displays composed of multiple display traits, and females are thought to use these different traits in mate choice. Models of multiple display trait evolution suggest that these traits provide females with different kinds of information in different stages of the mate choice process, or function as redundant signals to improve the accuracy of mate assessment. We suggest that complex male displays might also arise because of variation in female preferences for particular male display traits. The causes of female preference variation have received little attention, and the role of preference variation in shaping complex male displays is unclear. Here we show that in satin bowerbirds (Ptilonorhynchus violaceus) female mate choice is a multistage process, where females of different ages use different male display traits in successive stages. Age- and stage-specific female preferences may contribute to explaining the widespread occurrence of multifaceted male displays.     

Female choice selects for a viability-based male trait in pheasants

Recent theory on sexual selection suggests that females in species without paternal care choose mates by their secondary sexual characters because these indicate genotypic quality which will be transmitted to the offspring. These ideas are not yet empirically supported as data quantifying the relationship between female mate choice and female reproductive success are lacking. Only in one case, in Colias butterflies, has it been demonstrated unequivocally that females choose 'good genotypes' as mates and there is only one study, on Drosophila, demonstrating that mate choice increases one component of offspring fitness. Spur length of male pheasants (Phasianus colchicus) correlates with various fitness-related properties. We here present the first experimental field data showing that female pheasants select mates on the basis of male spur length and that female mate choice correlates with female reproductive success.     

Directional postcopulatory sexual selection revealed by artificial insemination

Postcopulatory sexual selection comprises both sperm competition, where the sperm from different males compete for fertilization, and cryptic female choice, where females bias sperm use in favour of particular males. Despite intense current interest in both processes as potential agents of directional sexual selection, few studies have attributed the success of attractive males to events that occur exclusively after insemination. This is because the interactions between pre- and post-insemination episodes of sexual selection can be important sources of variation in paternity. The use of artificial insemination overcomes this difficulty because it controls for variation in male fertilization success attributable to the female's perception of male quality, as well as effects due to mating order and the relative contribution of sperm from competing males. Here, we adopt this technique and show that in guppies, when equal numbers of sperm from two males compete for fertilization, relatively colourful individuals achieve greater parentage than their less ornamented counterparts. This finding indicates that precopulatory female mating preferences can be reinforced exclusively through postcopulatory processes occurring at a physiological level. Our analysis also revealed that relatively small individuals were advantaged in sperm competition, suggesting a possible trade-off between sperm competitive ability and body growth.     

Pigmentation and mate choice in Drosophila

Many species of the fruitfly Drosophila are either sexually dimorphic for abdominal pigmentation (the posterior segments in males are black and those of females have thin dark stripes) or sexually monomorphic for this pigmentation (both sexes show striping). Kopp et al. report a correlation in two Drosophila clades between the expression of the bric-à-brac (bab) gene, which represses male-specific pigmentation in D. melanogaster females, and the presence of sexually dimorphic pigmentation. They suggest that sexual selection acted to produce sexual dichromatism in Drosophila by altering the regulation of bab, on the grounds that D. melanogaster males show a strong mate preference for females with lightly pigmented abdomens, and that this discrimination helps to maintain sexual dichromatism by preventing males from wasting time by courting other (darkly pigmented) males. Here we show that the mate discrimination observed by Kopp et al. may in fact have resulted from the nature of the strains and comparisons they used in their study and so could be irrelevant to mate choice in nature.     

Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild

Females often mate with several males before producing offspring. Field studies of vertebrates suggest, and laboratory experiments on invertebrates confirm, that even when males provide no material benefits, polyandry can enhance offspring survival. This enhancement is widely attributed to genetic benefits that arise whenever paternity is biased towards males that sire more viable offspring. Field studies suggest that post-mating sexual selection biases fertilization towards genetically more compatible males and one controlled experiment has shown that, when females mate with close kin, polyandry reduces the relative number of inbred offspring. Another potential genetic benefit of polyandry is that it increases offspring survival because males with more competitive ejaculates sire more viable offspring. Surprisingly, however, there is no unequivocal evidence for this process. Here, by experimentally assigning mates to females, we show that polyandry greatly increases offspring survival in the Australian marsupial Antechinus stuartii. DNA profiling shows that males that gain high paternity under sperm competition sire offspring that are more viable. This beneficial effect occurs in both the laboratory and the wild. Crucially, there are no confounding non-genetic maternal effects that could arise if polyandry increases female investment in a particular reproductive event because A. stuartii is effectively semelparous. Our results therefore show that polyandry improves female lifetime fitness in nature. The threefold increase in offspring survival is not negated by a decline in maternal lifespan and is too large to be offset by an equivalent decline in the reproductive performance of surviving offspring.     

Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism.

The origin and maintenance of polymorphism in major histocompatibility complex (MHC) genes in natural populations is still unresolved. Sexual selection, frequency-dependent selection by parasites and pathogens, and heterozygote advantage have been suggested to explain the maintenance of high allele diversity at MHC genes. Here we argue that there are two (non-exclusive) strategies for MHC-related sexual selection, representing solutions to two different problems: inbreeding avoidance and parasite resistance. In species prone to inadvertent inbreeding, partners should prefer dissimilar MHC genotypes to similar ones. But if the goal is to maximize the resistance of offspring towards potential infections, the choosing sex should prefer mates with a higher diversity of MHC alleles. This latter strategy should apply when there are several MHC loci, as is the case in most vertebrates. We tested the relative importance of an 'allele counting' strategy compared to a disassortative mating strategy using wild-caught three-spined sticklebacks (Gasterosteus aculeatus) from an interconnected system of lakes. Here we show that gravid female fish preferred the odour of males with a large number of MHC class-IIB alleles to that of males with fewer alleles. Females did not prefer male genotypes dissimilar to their own.     

Intensity of sexual selection along the anisogamy-isogamy continuum

Research into the evolution of giant sperm has uncovered a paradox within the foundations of sexual selection theory. Postcopulatory sexual selection on males (that is, sperm competition and cryptic female choice) can lead to decreased sperm numbers by favouring the production of larger sperm. However, a decline in sperm numbers is predicted to weaken selection on males and increase selection on females. As isogamy is approached (that is, as investment per gamete by males approaches that by females), sperm become less abundant, ova become relatively less rare, and competition between males for fertilization success is predicted to weaken. Sexual selection for longer sperm, therefore, is expected to be self limiting. Here we examine this paradox in Drosophila along the anisogamy-isogamy continuum using intraspecific experimental evolution techniques and interspecific comparative techniques. Our results confirm the big-sperm paradox by showing that the sex difference in sexual selection gradients decreases as sperm size increases. However, a resolution to the paradox is provided when this finding is interpreted in concert with the 'opportunity for selection' and the 'opportunity for sexual selection'. Furthermore, we show that most of the variation in measures of selection intensity is explained by sperm length and relative investment in sperm production.     

Testing the genetics underlying the co-evolution of mate choice and ornament in the wild

One of the most debated questions in evolutionary biology is whether female choice of males with exaggerated sexual displays can evolve as a correlated response to selection acting on genes coding for male attractiveness or high overall viability. To date, empirical studies have provided support for parts of this scenario, but evidence for all key genetic components in a natural population is lacking. Here we use animal-model quantitative genetic analysis on data from over 8,500 collared flycatchers (Ficedula albicollis) followed for 24 years to quantify all of the key genetic requirements of both fisherian and 'good-genes' models on sexual selection in the wild. We found significant additive genetic variances of all the main components: male ornament (forehead patch size), female mate choice for this ornament, male fitness and female fitness. However, when the necessary genetic correlations between these components were taken into account, the estimated strength of indirect sexual selection on female mate choice was negligible. Our results show that the combined effect of environmental influences on several components reduces the potential for indirect sexual selection in the wild. This study provides insight into the field of sexual selection by showing that genes coding for mate choice for an ornament probably evolve by their own pathways instead of 'hitchhiking' with genes coding for the ornament.     

Female mate-choice drives the evolution of male-biased dispersal in a social mammal

Dispersal has a significant impact on lifetime reproductive success, and is often more prevalent in one sex than the other. In group-living mammals, dispersal is normally male-biased and in theory this sexual bias could be a response by males to female mate preferences, competition for access to females or resources, or the result of males avoiding inbreeding. There is a lack of studies on social mammals that simultaneously assess these factors and measure the fitness consequences of male dispersal decisions. Here we show that male-biased dispersal in the spotted hyaena (Crocuta crocuta) most probably results from an adaptive response by males to simple female mate-choice rules that have evolved to avoid inbreeding. Microsatellite profiling revealed that females preferred sires that were born into or immigrated into the female's group after the female was born. Furthermore, young females preferred short-tenured sires and older females preferred longer-tenured sires. Males responded to these female mate preferences by initiating their reproductive careers in groups containing the highest number of young females. As a consequence, 11% of males started their reproductive career in their natal group and 89% of males dispersed. Males that started reproduction in groups containing the highest number of young females had a higher long-term reproductive success than males that did not. The female mate-choice rules ensured that females effectively avoided inbreeding without the need to discriminate directly against close kin or males born in their own group, or to favour immigrant males. The extent of male dispersal as a response to such female mate preferences depends on the demographic structure of breeding groups, rather than the genetic relatedness between females and males.     

基于SSR分子标记检测褐飞虱交配次数及性选择

为探明褐飞虱交配次数和性选择的生殖行为特征,构建了褐飞虱生物型1和生物型Y的近交系,筛选了在不同近交系之间存在明显差异的9个SSR(Simple Sequence Repeats)分子标记用于亲子鉴定.在雌虫交配次数试验中,观察并分子鉴定到23头成功交配的雌虫,其中19头雌虫一生仅进行1次交配,4头雌虫一生进行了2次交...     

Female swallow preference for symmetrical male sexual ornaments.

Many secondary sexual characters are supposed to have evolved as a response to female choice of the most extravagantly ornamented males, a hypothesis supported by studies demonstrating female preferences for the most ornamented males. Comparative studies of elaborate feather ornaments in birds have shown that (1) ornaments have larger degrees of fluctuating asymmetry (small, random deviations from bilateral symmetry caused by an inability of individuals to cope with environmental and genetic stress during development of a character) than other morphological traits, and (2) the degree of fluctuating asymmetry is often negatively related to the size of the ornament. The negative relationship between ornament asymmetry and size suggests that ornament size reliably reflects male quality because the largest secondary sex traits demonstrate the least degree of fluctuating asymmetry. I manipulated tail length and tail asymmetry independently in male swallows (Hirundo rustica) to determine whether ornament size or asymmetry were used as cues in mate choice. Male swallows with elongated, symmetric tails mated earlier, and enjoyed larger annual reproductive success than did males with shortened tails and increased asymmetry. Females therefore prefer large as well as symmetric ornaments, which suggests that females in their mate choice use ornament asymmetry and size as reliable indicators of male quality.     

Mate guarding as paternity insurance in Idaho ground squirrels

Following a copulation, males in many species of vertebrates (particularly birds) and invertebrates remain near the inseminated female and repel other suitors with displays or force. Guarding males must delay resumption of competitive mate searching, but they may insure their paternity by reducing possibilities for secondary matings and sperm competition. Among mammals, post-copulatory mate guarding has been reported in rodents, mongooses, ungulates and primates, including humans, but the effects of such behaviour on male reproductive success have not been determined genetically. I report here that mate guarding by male Idaho ground squirrels (Spermophilus brunneus) enhances a male's probability of paternity. Furthermore, an analysis based on game theory shows that mate guarding is an evolutionarily stable strategy for male S. brunneus, but not male Belding's ground squirrels (S. beldingi), which resume searching once copulation is completed.     

Male displays adjusted to female's response.

Models of sexual selection generally assume that behavioural courtship displays reflect intrinsic male qualities such as condition, and that males display with maximum intensity to attract females to mate. Here we use robotic females in a field experiment to demonstrate that male satin bowerbirds (Ptilonorhynchus violaceus) do not always display at maximum intensity - rather, successful males modulate their displays in response to signals from females. Our results indicate that sexual selection may favour those males that can produce intense displays but which know how to modify these according to the female response.     

Sexual selection enables long-term coexistence despite ecological equivalence

Empirical data indicate that sexual preferences are critical for maintaining species boundaries, yet theoretical work has suggested that, on their own, they can have only a minimal role in maintaining biodiversity. This is because long-term coexistence within overlapping ranges is thought to be unlikely in the absence of ecological differentiation. Here we challenge this widely held view by generalizing a standard model of sexual selection to include two ubiquitous features of populations with sexual selection: spatial variation in local carrying capacity, and mate-search costs in females. We show that, when these two features are combined, sexual preferences can single-handedly maintain coexistence, even when spatial variation in local carrying capacity is so slight that it might go unnoticed empirically. This theoretical study demonstrates that sexual selection alone can promote the long-term coexistence of ecologically equivalent species with overlapping ranges, and it thus provides a novel explanation for the maintenance of species diversity.     

Paternal inheritance of a female moth's mating preference

Females of the arctiid moth Utetheisa ornatrix mate preferentially with larger males, receiving both direct phenotypic and indirect genetic benefits. Here we demonstrate that the female's mating preference is inherited through the father rather than the mother, indicating that the preference gene or genes lie mostly or exclusively on the Z sex chromosome, which is strictly paternally inherited by daughters. Furthermore, we show that the preferred male trait and the female preference for that trait are correlated, as females with larger fathers have a stronger preference for larger males. These findings are predicted by the protected invasion theory, which asserts that male homogametic sex chromosome systems (ZZ/ZW) found in lepidopterans and birds promote the evolution of exaggerated male traits through sexual selection. Specifically, the theory predicts that, because female preference alleles arising on the Z chromosome are transmitted to all sons that have the father's attractive trait rather than to only a fraction of the sons, such alleles will experience stronger positive selection and be less vulnerable to chance loss than would autosomal alleles.     

Outbred embryos rescue inbred half-siblings in mixed-paternity broods of live-bearing females

Females commonly mate with more than one male, and polyandry has been shown to increase reproductive success in many species. Insemination by multiple males shifts the arena for sexual selection from the external environment to the female reproductive tract, where sperm competition or female choice of sperm could bias fertilization against sperm from genetically inferior or genetically incompatible males. Evidence that polyandry can be a strategy for avoiding incompatibility comes from studies showing that inbreeding cost is reduced in some egg-laying species by postcopulatory mechanisms that favour fertilization by sperm from unrelated males. In viviparous (live-bearing) species, inbreeding not only reduces offspring genetic quality but might also disrupt feto-maternal interactions that are crucial for normal embryonic development. Here we show that polyandry in viviparous pseudoscorpions reduces inbreeding cost not through paternity-biasing mechanisms favouring outbred offspring, but rather because outbred embryos exert a rescuing effect on inbred half-siblings in mixed-paternity broods. The benefits of polyandry may thus be more complex for live-bearing females than for females that lay eggs.     

Genetic similarity between mates and extra-pair parentage in three species of shorebirds

Matings between close relatives often reduce the fitness of offspring, probably because homozygosity leads to the expression of recessive deleterious alleles. Studies of several animals have shown that reproductive success is lower when genetic similarity between parents is high, and that survival and other measures of fitness increase with individual levels of genetic diversity. These studies indicate that natural selection may favour the avoidance of matings with genetically similar individuals. But constraints on social mate choice, such as a lack of alternatives, can lead to pairing with genetically similar mates. In such cases, it has been suggested that females may seek extra-pair copulations with less related males, but the evidence is weak or lacking. Here we report a strong positive relationship between the genetic similarity of social pair members and the occurrence of extra-pair paternity and maternity ('quasi-parasitism') in three species of shorebirds. We propose that extra-pair parentage may represent adaptive behavioural strategies to avoid the negative effects of pairing with a genetically similar mate.