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.     

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 mating bias results in conflicting sex-specific offspring fitness

Indirect-benefit models of sexual selection assert that females gain heritable offspring advantages through a mating bias for males of superior genetic quality. This has generally been tested by associating a simple morphological quality indicator (for example, bird tail length) with offspring viability. However, selection acts simultaneously on many characters, limiting the ability to detect significant associations, especially if the simple indicator is weakly correlated to male fitness. Furthermore, recent conceptual developments suggest that the benefits gained from such mating biases may be sex-specific because of sexually antagonistic genes that differentially influence male and female reproductive ability. A more suitable test of the indirect-benefit model would examine associations between an aggregate quality indicator (such as male mating success) and gender-specific adult fitness components, under the expectation that these components may trade off. Here, we show that a father's mating success in the cricket, Allonemobius socius, is positively genetically correlated with his son's mating success but negatively with his daughter's reproductive success. This provides empirical evidence that a female mating bias can result in sexually antagonistic offspring fitness.     

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.     

Mating advantage of rare males in models of sexual selection

Models of sexual selection in polygynous species of animals have been derived on the assumption that some females have preferences to mate with males with particular genotypes. The mating advantage gained by the males is always frequency-dependent because the preferred males take part in the same number of preferential matings when they are rare as when they are common; individually therefore, they mate more often when they are rare. Frequency-dependent sexual selection has been demonstrated in many experiments with Drosophila: rare males take part in a higher proportion of matings than their frequency as available mates. Ehrman and Spiess explained this phenomenon by frequency-dependence either in female preference or in male courtship. This explanation, which is difficult to interpret in behavioural terms, may not be necessary, however, because constant female preferences would entail frequency-dependent selection among the males. I show here that a simple model of constant preferences for particular phenotypes or genotypes is sufficient to explain a large body of data on frequency-dependent sexual selection in Drosophila.     

Mate fidelity and intra-lineage polygyny in greater horseshoe bats

Mating strategies that lead to increased kinship within socially cooperative groups may offer inclusive fitness benefits to individuals, but can also result in higher levels of inbreeding. Here we show in a sexually segregated bat species that females avoid this conflict through two mating behaviours. First, most females revisit and breed with specific, individual males across years, so that their single offspring born in different years are full siblings. Second, relatives in the maternal line, including mothers and daughters, share breeding partners (intra-lineage polygyny) more often than expected by chance. Although these behaviours increased levels of co-ancestry among colony members, there was no concomitant rise in inbreeding. We suggest that when females engage in mate fidelity and intra-lineage polygyny, kin ties among female roost mates will be strengthened, thereby potentially contributing to social group cohesiveness. Our findings reveal the hidden complexity that can underlie polygynous breeding, and highlight a new potential route by which female mate choice could influence social evolution.     

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.     

Egg investment is influenced by male attractiveness in the mallard

Why females prefer to copulate with particular males is a contentious issue. Attention is currently focused on whether females choose males on the basis of their genetic quality, in order to produce more viable offspring. Support for this hypothesis in birds has come from studies showing that preferred males tend to father offspring of better condition or with increased survivorship. Before attributing greater offspring viability to a male's heritable genetic quality, however, it is important to discount effects arising from confounding sources, including maternal effects. This has generally been addressed by comparing offspring viability from two different breeding attempts by the same female: one when offspring are sired by a preferred male, and one when offspring are sired by a less preferred male. However, here we show that individual female mallard (Anas platyrhynchos) lay larger eggs after copulating with preferred males and smaller eggs after copulating with less preferred males. As a result, females produced offspring of better body condition when paired with preferred males. After controlling for these differences in maternal investment, we found no effect of paternity on offspring condition. This shows that differences between half-sibs cannot always be attributed to paternal or maternal genetic effects.     

Mate choice on fallow deer leks

Leks, on which males defend small clustered mating territories, may have evolved because of the unusual opportunities they provide for female choice of mating partners, and several studies of lek-breeding animals have demonstrated correlations between the mating success of males and their phenotype or behaviour. However, these could arise because (1) females select mates on the basis of male phenotypic traits; (2) males interfere with each other's mating attempts; or (3) females show preferences for particular mating territories, and larger or stronger males are more likely to win access to these territories. Here we report that when fallow bucks on a traditional lek were experimentally induced to change their territories, differences in the mating success of bucks persisted, whereas differences in the position of their territories relative to the centre of the lek did not. The observation that bucks rarely interfered with their neighbours' harems and females moved freely between bucks suggests that females choose their mates on the basis of male phenotype rather than territory type or location. In this population, the immediate factor affecting the movements of females between males was the size of a buck's harem.     

Female mimicry in garter snakes

In many diverse taxa, males of the same species often exhibit multiple mating strategies. One well-documented alternative male reproductive pattern is 'female mimicry', whereby males assume a female-like morphology or mimic female behaviour patterns. In some species males mimic both female morphology and behaviour. We report here female mimicry in a reptile, the red-sided garter snake (Thamnophis sirtalis parietalis). This form of mimicry is unique in that it is expressed as a physiological feminization. Courting male red-sided garter snakes detect a female-specific pheromone and normally avoid courting other males. However, a small proportion of males release a pheromone that attracts other males, as though they were females. In the field, mating aggregations of 5-17 males were observed formed around these individual attractive males, which we have termed 'she-males'. In competitive mating trails, she-males mated with females significantly more often than did normal males, demonstrating not only reproductive competence but also a possible selective advantage to males with this female-like pheromone.     

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.     

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.     

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.     

Population density affects sex ratio variation in red deer.

Many mammal populations show significant deviations from an equal sex ratio at birth, but these effects are notoriously inconsistent. This may be because more than one mechanism affects the sex ratio and the action of these mechanisms depends on environmental conditions. Here we show that the adaptive relationship between maternal dominance and offspring sex ratio previously demonstrated in red deer (Cervus elaphus), where dominant females produced more males, disappeared at high population density. The proportion of males born each year declined with increasing population density and with winter rainfall, both of which are environmental variables associated with nutritional stress during pregnancy. These changes in the sex ratio corresponded to reductions in fecundity, suggesting that they were caused by differential fetal loss. In contrast, the earlier association with maternal dominance is presumed to have been generated pre-implantation. The effects of one source of variation superseded the other within about two generations. Comparison with other ungulate studies indicates that positive associations between maternal quality and the proportion of male offspring born have only been documented in populations below carrying capacity.     

Sperm competition: motility and the midpiece in primates

In animals with multiple-partner mating systems, the gametes of two or more males must compete to fertilize a given set of ova. Here we show that the volume of the midpiece in individual sperm is significantly greater in primate species in which the females mate with multiple partners, and in which males have larger testes in relation to their body weight, than in those species that mate with only one partner and have relatively small testes. Our results indicate that sexual selection by sperm competition has influenced the evolution of a specific component of male-gamete morphology, the volume of the sperm midpiece.     

Roaring by red deer stags advances the date of oestrus in hinds

Some male mammals call loudly and repeatedly during the breeding season. Although the song of male birds is known to have effects on male-male competition, mate selection and ovulation, until now the loud calls of male mammals have been shown to affect only competition between males. Although it has been suggested that loud calling could also serve to attract females, the possibility that it has a direct effect on reproduction in females has not previously been investigated for any mammal. Here I report that roaring in red deer (Cervus elaphus) advances ovulation and that harem-holding males can improve their mating success by regular calling.     

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.     

Sexual conflict reduces offspring fitness in zebra finches

Parental care is often costly; hence, in sexually reproducing species where both male and female parents rear their offspring (biparental care), sexual conflict over parental investment can arise. Such conflict occurs because each care-giver would benefit from withholding parental investment for use with another partner, leading to a reduction in the amount of care given by one parent at the expense of the other. Here we report experiments to explore the prediction from theory that parents rearing offspring alone may provide greater parental investment than when rearing offspring together with a partner. We found that when the number of offspring per parent, and hence the potential workload, were kept constant, offspring received a greater per capita parental investment from single females than from both parents working together, and that males reared by single mothers were more sexually attractive as adults than their biparentally reared siblings. This difference between single- and two-parent families is due to a reduction in care provided by females when they care together with a male, rather than laziness by males or differences in the begging behaviour of chicks, supporting the claim that sexual conflict in biparental care can reduce the quality of offspring raised.     

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.     

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...