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.     

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.     

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.     

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.     

Sperm competition between Drosophila males involves both displacement and incapacitation.

Females in almost all animal groups copulate with multiple males. This behaviour allows different males to compete for fertilization and gives females the opportunity to mediate this competition. In many animals and most insects, the second male to copulate with a female typically sires most of her offspring. In Drosophila melanogaster, this second-male sperm precedence has long been studied but, as in most species, its mechanism has remained unknown. Here we show, using labelled sperm in doubly mated females, that males can both physically displace and incapacitate stored sperm from earlier-mating males. Displacement occurs only if the second male transfers sperm to the female, and in only one of her three sperm-storage organs. Incapacitation can be caused by either fertile or spermless second males, but requires extended intervals between matings. Sperm from different males are not 'stratified' in the storage organs but mix freely. Many animal species may have multiple mechanisms of sperm competition like those observed here, and revealing these mechanisms is necessary to understand the genetic and evolutionary basis of second-male sperm precedence in animals.     

Clonal reproduction by males and females in the little fire ant

Sexual reproduction can lead to major conflicts between sexes and within genomes. Here we report an extreme case of such conflicts in the little fire ant Wasmannia auropunctata. We found that sterile workers are produced by normal sexual reproduction, whereas daughter queens are invariably clonally produced. Because males usually develop from unfertilized maternal eggs in ants and other haplodiploid species, they normally achieve direct fitness only through diploid female offspring. Hence, although the clonal production of queens increases the queen's relatedness to reproductive daughters, it potentially reduces male reproductive success to zero. In an apparent response to this conflict between sexes, genetic analyses reveal that males reproduce clonally, most likely by eliminating the maternal half of the genome in diploid eggs. As a result, all sons have nuclear genomes identical to those of their father. The obligate clonal production of males and queens from individuals of the same sex effectively results in a complete separation of the male and female gene pools. These findings show that the haplodiploid sex-determination system provides grounds for the evolution of extraordinary genetic systems and new types of sexual conflict.     

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.     

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.     

Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species

Post-mating mechanisms are central to the establishment of reproductive isolation between different, but closely related, species. Post-mating isolation mechanisms include hybrid breakdown, hybrid sterility and hybrid lethality and may, in some cases, be reinforced by pre-mating mechanisms such as ethological differentiation. In the Drosophila melanogaster species sub-group post-mating reproductive isolation is ensured by both the inviability and the sterility of hybrids. For example when D. melanogaster females are crossed to D. simulans males the hybrid progeny are normally all female; the hybrid males die as third instar larvae. The viable hybrid females are totally sterile. Little is known of the genetic basis for either hybrid sterility or hybrid inviability, although Coyne and others have begun a genetic analysis of the sterility of hybrids within this species sub-group. We have discovered a single gene difference that rescues the otherwise inviable male hybrids from the cross between D. melanogaster females and males of its three closest relatives. The study of this locus may shed light on the genetic control of both speciation and development.     

Female transference and mate choice among Tana River red colobus.

Red colobus are one of a small number of primate species in which females have been reported to transfer between breeding groups more commonly than males. Several authors have hypothesised that in such species transference may serve to reduce the risk to females of producing offspring of lower fitness through inbreeding. The hypothesis offers no explanation of why females rather than males are responsible for outbreeding in these species, but remains plausible so long as male membership of breeding groups is relatively stable; for once members of one sex have evolved dispersal mechanisms reducing the risk of inbreeding, pressures on the other sex to do likewise will be lowered. Hence, if both sexes commonly migrate, the hypothesis is weakened. I describe here the membership dynamics of a group of Tana River red colobus, Colobus badius rufomitratus, which provide the first evidence of high rates of membership turnover by both sexes in primates, and speculate that the function of female transference in this case may be related to mate choice and the avoidance of infanticide.     

Female fur seals show active choice for males that are heterozygous and unrelated

Much debate surrounds the exact rules that influence mating behaviour, and in particular the selective forces that explain the evolution of female preferences. A key example is the lek paradox, in which female choice is expected rapidly to become ineffective owing to loss of additive genetic variability for the preferred traits. Here we exploit a remarkable system in which female fur seals exert choice by moving across a crowded breeding colony to visit largely static males. We show that females move further to maximize the balance between male high multilocus heterozygosity and low relatedness. Such a system shows that female choice can be important even in a strongly polygynous species, and at the same time may help to resolve the lek paradox because heterozygosity has low heritability and inbreeding avoidance means there is no single 'best' male for all females.     

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.     

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.     

Evidence that sensory traps can evolve into honest signals

Conventional models explaining extreme sexual ornaments propose that these reflect male genetic quality or are arbitrary results of genetic linkage between female preference and the ornament. The chase-away model emphasizes sexual conflict: male signals attract females because they exploit receiver biases. As males gain control of mating decisions, females may experience fitness costs through suboptimal mating rates or post-copulatory exploitation. Elaboration of male signals is expected if females increase their response threshold to resist such exploitation. If ornaments target otherwise adaptive biases such as feeding responses, selection on females might eventually separate sexual and non-sexual responses to the signal. Here we show that the terminal yellow band (TYB) of several Goodeinae species evokes both feeding and sexual responses; sexual responsiveness phylogenetically pre-dates the expression of the TYB in males and is comparable across taxa, yet feeding responsiveness decreases in species with more elaborated TYBs. Displaying a TYB is costly, and thus provides an example where a trait arose as a sensory trap but has evolved into an honest signal.     

Sophisticated sperm allocation in male fowl

When a female is sexually promiscuous, the ejaculates of different males compete for the fertilization of her eggs; the more sperm a male inseminates into a female, the more likely he is to fertilize her eggs. Because sperm production is limited and costly, theory predicts that males will strategically allocate sperm (1) according to female promiscuity, (2) saving some for copulations with new females, and (3) to females producing more and/or better offspring. Whether males allocate sperm in all of these ways is not known, particularly in birds where the collection of natural ejaculates only recently became possible. Here we demonstrate male sperm allocation of unprecedented sophistication in the fowl Gallus gallus. Males show status-dependent sperm investment in females according to the level of female promiscuity; they progressively reduce sperm investment in a particular female but, on encountering a new female, instantaneously increase their sperm investment; and they preferentially allocate sperm to females with large sexual ornaments signalling superior maternal investment. Our results indicate that female promiscuity leads to the evolution of sophisticated male sexual behaviour.     

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.     

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.     

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.     

The genetic basis of Haldane's rule

'Haldane's rule', formulated by J. B. S. Haldane in 1922, states that: "When in the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous [heterogametic] sex". His rule is now known to apply in mammals, lepidopterans, birds, orthopterans and dipterans. In Drosophila, for example, Bock cites 142 cases of interspecific hybridizations that produce one sterile and one fertile sex in the offspring, all but one of these crosses yielding sterile XY males and fertile XX females. Despite much speculation, however, the genetic basis of Haldane's rule remains unknown. Haldane himself rejected the simple explanation that males are innately more sensitive than females to the effects of hybridization because groups with heterogametic females (such as birds and butterflies) usually show female sterility in hybrids, so that heterogamety itself is the critical feature. He and others suggested that heterogametic infertility or inviability in hybrids arises by a genetic imbalance between X chromosomes and autosomes. An alternative explanation is that this syndrome is caused by a mismatch of X and Y chromosomes. Here I show that in the Drosophila melanogaster subgroup, Haldane's rule for fertility apparently arises from a genetic interaction between X and Y chromosomes and not from an imbalance between sex chromosomes and autosomes. This finding has important implications for understanding the evolution of interspecific reproductive isolation.