Negative genetic correlation between male sexual attractiveness and survival

Indirect selection of female mating preferences may result from a genetic association between male attractiveness and offspring fitness. The offspring of attractive males may have enhanced growth, fecundity, viability or attractiveness. However, the extent to which attractive males bear genes that reduce other fitness components has remained unexplored. Here I show that sexual attractiveness in male guppies (Poecilia reticulata) is heritable and genetically correlated with ornamentation. Like ornamentation, attractiveness may be substantially Y-linked. The benefit of mating with attractive males, and thus having attractive sons, is opposed by strong negative genetic correlation between attractiveness and both offspring survival and the number of sons maturing. Such correlations suggest either antagonistic pleiotropy between attractiveness and survival or linkage disequilibrium between attractive and deleterious alleles. The presence of many colour pattern genes on or near the non-recombining section of the Y chromosome may facilitate the accumulation of deleterious mutations by genetic hitchhiking. These findings show that genes enhancing sexual attractiveness may be associated with pleiotropic costs or heavy mutational loads.     

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.     

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.     

Sexually antagonistic genetic variation for fitness in red deer

Evolutionary theory predicts the depletion of genetic variation in natural populations as a result of the effects of selection, but genetic variation is nevertheless abundant for many traits that are under directional or stabilizing selection. Evolutionary geneticists commonly try to explain this paradox with mechanisms that lead to a balance between mutation and selection. However, theoretical predictions of equilibrium genetic variance under mutation-selection balance are usually lower than the observed values, and the reason for this is unknown. The potential role of sexually antagonistic selection in maintaining genetic variation has received little attention in this debate, surprisingly given its potential ubiquity in dioecious organisms. At fitness-related loci, a given genotype may be selected in opposite directions in the two sexes. Such sexually antagonistic selection will reduce the otherwise-expected positive genetic correlation between male and female fitness. Both theory and experimental data suggest that males and females of the same species may have divergent genetic optima, but supporting data from wild populations are still scarce. Here we present evidence for sexually antagonistic fitness variation in a natural population, using data from a long-term study of red deer (Cervus elaphus). We show that male red deer with relatively high fitness fathered, on average, daughters with relatively low fitness. This was due to a negative genetic correlation between estimates of fitness in males and females. In particular, we show that selection favours males that carry low breeding values for female fitness. Our results demonstrate that sexually antagonistic selection can lead to a trade-off between the optimal genotypes for males and females; this mechanism will have profound effects on the operation of selection and the maintenance of genetic variation in natural populations.     

Rapid evolution of reproductive barriers driven by sexual conflict

A growing amount of experimental data indicates extremely rapid evolution of traits and proteins related to fertilization in many diverging taxa. These data come from studies of sperm or pollen competition between closely related species, and from molecular studies of fertilization proteins. The positive selection for evolutionary novelty that appears to be acting on fertilization systems seems paradoxical because successful reproduction requires the close matching of female and male traits. It has been suggested that perpetual coevolution between the sexes can result from sexual conflict in mating. Sexual conflict occurs when characteristics that enhance the reproductive success of one sex reduce the fitness of the other sex. Numerous examples of sexual conflict resulting from sensory exploitation, polyspermy and the cost of mating have been discussed in detail. The potential for coevolution due to such conflict has been evaluated experimentally. Here I develop a simple mathematical model describing coevolutionary dynamics of male and female traits involved in reproduction. The model shows that continual change in such traits at a constant speed is expected whenever females (or eggs) experience fitness loss from having too many compatible males (or sperms). The plausibility of runaway coevolution increases with increasing population size. Rapid evolution of reproductive barriers driven by sexual conflict may explain increased speciation rates after colonization of new habitats ('adaptive radiation') and high species richness in resource-rich environments.     

Fitness benefits of prolonged post-reproductive lifespan in women

Most animals reproduce until they die, but in humans, females can survive long after ceasing reproduction. In theory, a prolonged post-reproductive lifespan will evolve when females can gain greater fitness by increasing the success of their offspring than by continuing to breed themselves. Although reproductive success is known to decline in old age, it is unknown whether women gain fitness by prolonging lifespan post-reproduction. Using complete multi-generational demographic records, we show that women with a prolonged post-reproductive lifespan have more grandchildren, and hence greater fitness, in pre-modern populations of both Finns and Canadians. This fitness benefit arises because post-reproductive mothers enhance the lifetime reproductive success of their offspring by allowing them to breed earlier, more frequently and more successfully. Finally, the fitness benefits of prolonged lifespan diminish as the reproductive output of offspring declines. This suggests that in female humans, selection for deferred ageing should wane when one's own offspring become post-reproductive and, correspondingly, we show that rates of female mortality accelerate as their offspring terminate reproduction.     

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.     

Hybridization and adaptive mate choice in flycatchers

Hybridization in natural populations is strongly selected against when hybrid offspring have reduced fitness. Here we show that, paradoxically, pairing with another species may offer the best fitness return for an individual, despite reduced fitness of hybrid offspring. Two mechanisms reduce the costs to female collared flycatchers of pairing with male pied flycatchers. A large proportion of young are sired by conspecific male collared flycatchers through extra-pair copulations, and there is a bias in favour of male offspring (which, unlike females, are fertile) within hybrid pairs. In combination with temporal variation in breeding success, these cost-reducing mechanisms yield quantitative predictions about when female collared flycatchers should accept a male pied flycatcher as a mate; empirical data agree with these predictions. Apparent hybridization may thus represent adaptive mate choice under some circumstances.     

Parthenogenesis in Komodo dragons

Parthenogenesis, the production of offspring without fertilization by a male, is rare in vertebrate species, which usually reproduce after fusion of male and female gametes. Here we use genetic fingerprinting to identify parthenogenetic offspring produced by two female Komodo dragons (Varanus komodoensis) that had been kept at separate institutions and isolated from males; one of these females subsequently produced additional offspring sexually. This reproductive plasticity indicates that female Komodo dragons may switch between asexual and sexual reproduction, depending on the availability of a mate--a finding that has implications for the breeding of this threatened species in captivity. Most zoos keep only females, with males being moved between zoos for mating, but perhaps they should be kept together to avoid triggering parthenogenesis and thereby decreasing genetic diversity.     

Divergent sexual selection enhances reproductive isolation in sticklebacks

Sexual selection may facilitate speciation because it can cause rapid evolutionary diversification of male mating signals and female preferences. Divergence in these traits can then contribute to reproductive isolation. The sensory drive hypothesis predicts that three mechanisms underlie divergence in sexually selected traits: (1) habitat-specific transmission of male signals; (2) adaptation of female perceptual sensitivity to local ecological conditions; and (3) matching of male signals to female perceptual sensitivity. I test these mechanisms in threespine sticklebacks (Gasterosteus spp.) that live in different light environments. Here I show that female perceptual sensitivity to red light varies with the extent of redshift in the light environment, and contributes to divergent preferences. Male nuptial colour varies with environment and is tuned to female perceptual sensitivity. The extent of divergence among populations in both male signal colour and female preference for red is correlated with the extent of reproductive isolation in these recently diverged species. These results demonstrate that divergent sexual selection generated by sensory drive contributes to speciation.     

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.     

Mutual mate choice in the Asiatic toad, Bufo gargarizans, exerts stabilizing selection on body size

Sexual selection is critical to both reproduction and evolution.The effects of male–male competition and female choice regarding body size have been examined in a large number of taxa,including toad species.Males and females have different optimal reproductive strategies,achieving breeding advantages in discrepant ways.Further,the relative contributions of intra-and inter-sexual size selection vary among species.Thus,to understand the mechanisms affecting mating success,it is important to consider both male–male and male–female interactions simultaneously and elucidate their interrelationship.In this study,we measured body sizes of all mated and unmated individuals in a population of Asiatic toad(Bufo gargarizans)and counted fertilized eggs of several clutches.Based on correlation and regression techniques,we tested for female choice and intra-sexual competition among males relative to body size gradients,and we compared the relative importance of these two processes for mating success.Our results reveal that male–male competition and female choice simultaneously contribute to sexual selection in toads.Furthermore,both interactions are most intense among smaller toads.The synergistic trends of male–male competition and female choice support the mutual mate choice hypothesis and works to stabilize body size in B.gargarizans.Normal distributions of breeding success relative to body size were detected for both sexes,suggesting that medium-sized individuals enjoy a reproductive advantage in the population studied.     

Sexual selection and the maintenance of sex

Sex is expensive. A population of females that reproduce asexually should prima facie have twice the growth rate of an otherwise equivalent anisogamous sexual population lacking paternal care, or a population with modes of paternal care that can be co-opted by parthenogenetic females. The two leading theories for the maintenance of sex require either synergistic interactions between deleterious mutations, or antagonistic epistasis between beneficial mutations. Current evidence is equivocal as to whether the required levels of epistasis exist. Here I show that a third factor, differential male mating success (or, more generally, higher variance in male than in female fitness), can drastically reduce mutational load in sexual populations with or without any form of epistasis. Differential mating success has the further advantage of being ubiquitous, and is likely to have preceded or evolved concurrently with anisogamy.     

Male mammals respond to a risk of sperm competition conveyed by odours of conspecific males

Sperm competition occurs when a female copulates with two or more males and the sperm of those males compete within the female's reproductive tract to fertilize her eggs. The frequent occurrence of sperm competition has forced males of many species to develop different strategies to overcome the sperm of competing males. A prevalent strategy is for males to increase their sperm investment (total number of sperm allocated by a male to a particular female) after detecting a risk of sperm competition. It has been shown that the proportion of sperm that one male contributes to the sperm pool of a female is correlated with the proportion of offspring sired by that male. Therefore, by increasing his sperm investment a male may bias a potential sperm competition in his favour. Here we show that male meadow voles, Microtus pennsylvanicus, increase their sperm investment when they mate in the presence of another male's odours. Such an increase in sperm investment does not occur by augmenting the frequency of ejaculations, but by increasing the amount of sperm in a similar number of ejaculations.     

Mating patterns in seminatural populations of mice influenced by MHC genotype

Because of the central role of major histocompatibility complex (MHC) genes in immune recognition, it is often assumed that parasite-driven selection maintains the unprecendented genetic diversity of these genes. But associations between MHC genotype and specific infectious diseases have been difficult to identify with a few exceptions such as Marek's disease and malaria. Alternatively, MHC-related reproductive mechanisms such as selective abortion and mating preferences could be responsible for the diversity. To determine both the nature and strength of selection operating on MHC genes by we have studied components of selection in seminatural populations of mice (Mus musculus domesticus). Here we assess MHC-related patterns of reproduction and early (preweaning) mortality by analysing 1,139 progeny born in nine populations, and 662 progeny from laboratory matings. Reproductive mechanisms, primarily mating preferences, result in 27% fewer MHC-homozygous offspring than expected from random mating. MHC genotype had no detectable influence on neonatal (preweaning) mortality. These mating preferences are strong enough to account for most of the MHC genetic diversity found in natural populations of Mus.     

Mammalian sex ratios and variation in costs of rearing sons and daughters

In red deer, the sex ratio of calves at birth (calculated as the proportion of calves born that are male) increases with the dominance rank of the mother, whereas opposite trends exist in several populations of macaques and baboons. Here we show that the subsequent survival and reproductive success of subordinate female red deer is depressed more by rearing sons than by rearing daughters, whereas the subsequent fitness of dominant females is unaffected by the sex of their present offspring. By contrast, among subordinate female macaques, the rearing of daughters has greater costs to the mother's subsequent fitness than does the rearing of sons, although again, no difference in the costs of rearing sons and daughters is found among dominant mothers. These findings indicate that both differences in the relative fitness of sons and daughters and differences in the relative costs of rearing male and female offspring can favour variation in the sex ratio.     

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.     

The adaptive significance of temperature-dependent sex determination in a reptile

Understanding the mechanisms that determine an individual's sex remains a primary challenge for evolutionary biology. Chromosome-based systems (genotypic sex determination) that generate roughly equal numbers of sons and daughters accord with theory, but the adaptive significance of environmental sex determination (that is, when embryonic environmental conditions determine offspring sex, ESD) is a major unsolved problem. Theoretical models predict that selection should favour ESD over genotypic sex determination when the developmental environment differentially influences male versus female fitness (that is, the Charnov-Bull model), but empirical evidence for this hypothesis remains elusive in amniote vertebrates--the clade in which ESD is most prevalent. Here we provide the first substantial empirical support for this model by showing that incubation temperatures influence reproductive success of males differently than that of females in a short-lived lizard (Amphibolurus muricatus, Agamidae) with temperature-dependent sex determination. We incubated eggs at a variety of temperatures, and de-confounded sex and incubation temperature by using hormonal manipulations to embryos. We then raised lizards in field enclosures and quantified their lifetime reproductive success. Incubation temperature affected reproductive success differently in males versus females in exactly the way predicted by theory: the fitness of each sex was maximized by the incubation temperature that produces that sex. Our results provide unequivocal empirical support for the Charnov-Bull model for the adaptive significance of temperature-dependent sex determination in amniote vertebrates.     

Sexual swellings advertise female quality in wild baboons

The females of many Old World primate species produce prominent and conspicuous swellings of the perineal skin around the time of ovulation. These sexual swellings have been proposed to increase competition among males for females or to increase the likelihood of a female getting fertilized, by signalling either a female's general reproductive status, or the timing of her ovulation. Here we show that sexual swellings in wild baboons reliably advertise a female's reproductive value over her lifetime, in accordance with a theoretical model of honest signalling. Females with larger swellings attained sexual maturity earlier, produced both more offspring and more surviving offspring per year than females with smaller swellings, and had a higher overall proportion of their offspring survive. Male baboons use the size of the sexual swelling to determine their mating effort, fighting more aggressively to consort females with larger swellings, and spending more time grooming these females. Our results document an unusual case of a sexually selected ornament in females, and show how males, by mating selectively on the basis of the size of the sexual swelling, increase their probability of mating with females more likely to produce surviving offspring.     

Post-mating clutch piracy in an amphibian

Female multiple mating and alternative mating systems can decrease the opportunity for sexual selection. Sperm competition is often the outcome of females mating with multiple males and has been observed in many animals, and alternative reproductive systems are widespread among species with external fertilization and parental care. Multiple paternity without associated complex behaviour related to mating or parental care is also seen in simultaneously spawning amphibians and fishes that release gametes into water. Here we report 'clutch piracy' in a montane population of the common frog Rana temporaria, a reproductive behaviour previously unknown in vertebrates with external fertilization. Males of this species clasp the females and the pair deposits one spherical clutch of eggs. No parental care is provided. 'Pirate' males search for freshly laid clutches, clasp them as they would do a female and fertilize the eggs that were left unfertilized by the 'parental' male. This behaviour does not seem to be size-dependent, and some males mate with a female and perform clutch piracy in the same season. Piracy affected 84% of the clutches and in some cases increased the proportion of eggs fertilized, providing direct fitness benefits both for the pirate males and the females. Sexual selection--probably caused by a strong male-biased sex ratio--occurs in this population, as indicated by size-assortative mating; however, clutch piracy may reduce its impact. This provides a good model to explore how alternative mating strategies can affect the intensity of sexual selection.