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.     

Antagonistic coevolution between the sexes in a group of insects

In coevolutionary 'arms races' between the sexes, the outcome of antagonistic interactions may remain at an evolutionary standstill. The advantage gained by one sex, with any evolutionary exaggeration of arms, is expected to be matched by analogous counteradaptations in the other sex. This fundamental coevolutionary process may thus be hidden from the evolutionist's eye, and no natural examples are known. We have studied the effects of male and female armament (clasping and anti-clasping morphologies) on the outcome of antagonistic mating interactions in 15 species of water strider, using a combination of experimental and phylogenetic comparative methods. Here we present, by assessing the independent effects of both species-specific level of arms escalation and small imbalances in the amounts of arms between the sexes within species, the consequences of a sexual arms race. Evolutionary change in the balance of armament between males and females, but not in the species-specific level of escalation, has resulted in evolutionary change in the outcome of sexually antagonistic interactions such as mating rate.     

Sex differences in emigration and mortality affect optimal management of deer populations

Populations of red deer that are limited by food, like those of many other ungulates, commonly include more females than males. We assessed the contribution of variation in sex- and age-specific rates of mortality and emigration to density-dependent changes in the adult sex ratio, using long-term observations and demographic experiments involving the red deer population on Rum, Scotland. We incorporated these effects in a stochastic model of local populations under different management regimes to show here that, when female numbers are allowed to increase to more than 60% of the ecological carrying capacity, the sustainable annual harvest of males from local deer populations will fall. Because males are typically culled by fee-paying hunters and generate more income than females, income will decrease as the male harvest falls. Because numbers of female deer throughout much of the Highlands probably exceed the threshold at which male density starts to be affected, many managers might be able to raise income from local deer populations by reducing female numbers, with potential benefits to the vegetation of Scottish Highland environments.     

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.     

Relative fitness can decrease in evolving asexual populations of S. cerevisiae

It is generally accepted from the darwinian theory of evolution that a progressive increase in population adaptation will occur in populations containing genetic variation in fitness, until a stable equilibrium is reached and/or the additive genetic variation is exhausted. However, the theoretical literature of population genetics documents exceptions where mean population fitness may decrease in response to evolutionary changes in gene frequency, due to varying selective coefficients, sexual selection or to epistatic interactions between loci. Until now, no examples of such exceptions have been documented from fitness estimates in either natural or experimental populations. We present here direct evidence that, as a result of epistatic interactions between adaptive mutations, mean population fitness can decrease in asexual evolving populations of the yeast Saccharomyces cerevisiae.     

Genetic basis of fitness differences in natural populations

Genomics profoundly influences current biology. One of many exciting consequences of this revolution is the potential for identifying and studying the genetic basis of those traits affecting fitness that are key to natural selection. Recent studies using a multitude of genomic approaches have established such genotype-phenotype relationships in natural populations, giving new insight into the genetic architecture of quantitative variation. In parallel, an emerging understanding of the quantitative genetics of fitness variation in the wild means that we are poised to see a synthesis of ecological and molecular approaches in evolutionary biology.     

Sexual selection and the maintenance of sexual reproduction

The maintenance of sexual reproduction is a problem in evolutionary theory because, all else being equal, asexual populations have a twofold fitness advantage over their sexual counterparts and should rapidly outnumber a sexual population because every individual has the potential to reproduce. The twofold cost of sex exists because of anisogamy or gamete dimorphism-egg-producing females make a larger contribution to the zygote compared with the small contribution made by the sperm of males, but both males and females contribute 50% of the genes. Anisogamy also generates the conditions for sexual selection, a powerful evolutionary force that does not exist in asexual populations. The continued prevalence of sexual reproduction indicates that the 'all else being equal' assumption is incorrect. Here I show that sexual selection can mitigate or even eliminate the cost of sex. If sexual selection causes deleterious mutations to be more deleterious in males than females, then deleterious mutations are maintained at lower equilibrium frequency in sexual populations relative to asexual populations. The fitness of sexual females is higher than asexuals because there is no difference in the fecundity of sexual females and asexuals of the same genotype, but the equilibrium frequency of deleterious mutations is lower in sexual populations. The results are not altered by synergistic epistasis in males.     

Disposable-soma senescence mediated by sexual selection in an ungulate

Senescence may result from an optimal balance between current reproductive investment and bodily repair processes required for future reproduction, a theoretical prediction difficult to prove especially in large, long-lived animals. Here we propose that teeth that have fixed dimensions early in life, but that wear during chewing, can be taken as a measure of total lifetime 'repair', and their wear rate as a measure of current expenditure in performance. Our approach also considers the sexual selection process to investigate the advance of senescence in males compared with females, when selection favouring competition over mates reduces the reproductive lifespan of males. We studied carcasses of 2,141 male and 739 female red deer (Cervus elaphus) of different ages, finding that male molariform teeth emerged at a far smaller size than expected from body size dimorphism. This led to higher workload, steeper wear rate and earlier depletion of male teeth than in females, in concordance with sex-specific patterns of lifetime performance and reproduction. These findings provide the empirical support for the disposable-soma hypothesis of senescence, which predicts that investment in bodily repair will decrease when the return from this investment may not be realized as a result of other causes that limit survival or reproduction.     

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.     

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.     

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.     

Fine-scale genetic structuring on Manacus manacus leks

Leks have traditionally been considered as arenas where males compete to attract females and secure matings. Thus, direct fitness benefits mediated through competition between males to fertilize females have been considered to be the primary force driving the evolution of lekking behaviour. Inclusive fitness benefits mediated through kin selection may also be involved in lek formation and evolution, but to date this theory has been largely ignored. According to kin-selection theory, both reproducing and non-reproducing males may gain indirect inclusive fitness benefits. If females are attracted to larger leks, non-reproducing males add attractiveness to a lek, and therefore, in a genetically structured population, boost the reproductive success of kin. Theory predicts that the attractiveness of leks is plastic, and that males establish themselves on a lek in which the top male, in terms of reproductive success, is a close relative. Here we show that in white-bearded manakins (Manacus manacus), for which larger leks are more attractive to females and so secure the maximum number of matings, there is extraordinary fine-scale genetic structure, with leks being composed of clusters of related kin. We propose that males establish themselves where they find relatives to such an extent that they form groups within leks, and that such behaviour is consistent with kin-selection theory to maximize reproductive success of the group.     

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.     

Frequency-dependent survival in natural guppy populations

The maintenance of genetic variation in traits under natural selection is a long-standing paradox in evolutionary biology. Of the processes capable of maintaining variation, negative frequency-dependent selection (where rare types are favoured by selection) is the most powerful, at least in theory; however, few experimental studies have confirmed that this process operates in nature. One of the most extreme, unexplained genetic polymorphisms is seen in the colour patterns of male guppies (Poecilia reticulata). Here we manipulated the frequencies of males with different colour patterns in three natural populations to estimate survival rates, and found that rare phenotypes had a highly significant survival advantage compared to common phenotypes. Evidence from humans and other species implicates frequency-dependent survival in the maintenance of molecular, morphological and health-related polymorphisms. As a controlled manipulation in nature, this study provides unequivocal support for frequency-dependent survival--an evolutionary process capable of maintaining extreme polymorphism.     

Host-parasite 'Red Queen' dynamics archived in pond sediment

Antagonistic interactions between hosts and parasites are a key structuring force in natural populations, driving coevolution. However, direct empirical evidence of long-term host-parasite coevolution, in particular 'Red Queen' dynamics--in which antagonistic biotic interactions such as host-parasite interactions can lead to reciprocal evolutionary dynamics--is rare, and current data, although consistent with theories of antagonistic coevolution, do not reveal the temporal dynamics of the process. Dormant stages of both the water flea Daphnia and its microparasites are conserved in lake sediments, providing an archive of past gene pools. Here we use this fact to reconstruct rapid coevolutionary dynamics in a natural setting and show that the parasite rapidly adapts to its host over a period of only a few years. A coevolutionary model based on negative frequency-dependent selection, and designed to mimic essential aspects of our host-parasite system, corroborated these experimental results. In line with the idea of continuing host-parasite coevolution, temporal variation in parasite infectivity changed little over time. In contrast, from the moment the parasite was first found in the sediments, we observed a steady increase in virulence over time, associated with higher fitness of the parasite.     

Adaptive plasticity in mate preference linked to differences in reproductive effort

There is abundant evidence for the existence of marked mate preferences in natural populations, but the occurrence of within-population variation in mate preferences has received little attention and is often regarded as nonadaptive deviation from the optimal norm. Here we show experimentally that the preference of female collared flycatchers Ficedula albicollis for male forehead patch size, a sexually selected trait, varies with the time of breeding, an environmental factor with strong effects on reproductive success. Contrary to expectations based on time-constrained choice models, only late-breeding females prefer males with a large patch size. The variation in mate preference matches a seasonal change in female reproductive success: long-term data reveal a positive relationship between female reproductive success and male patch size exclusively in late breeders. In addition, female reproductive effort, as assessed by clutch size, appears to be adjusted relative to both timing of breeding and male phenotype. We conclude that not only can mate preferences display adaptive plasticity within populations, but this plasticity can also be linked to differences in reproductive investment.     

Evolvability of an RNA virus is determined by its mutational neighbourhood

The ubiquity of mechanisms that generate genetic variation has spurred arguments that evolvability, the ability to generate adaptive variation, has itself evolved in response to natural selection. The high mutation rate of RNA viruses is postulated to be an adaptation for evolvability, but the paradox is that whereas some RNA viruses evolve at high rates, others are highly stable. Here we show that evolvability in the RNA bacteriophage phi6 is also determined by the accessibility of advantageous genotypes within the mutational neighbourhood (the set of mutants one or a few mutational steps away). We found that two phi6 populations that were derived from a single ancestral phage repeatedly evolved at different rates and toward different fitness maxima. Fitness measurements of individual phages showed that the fitness distribution of mutants differed between the two populations. Whereas population A, which evolved toward a higher maximum, had a distribution that contained many advantageous mutants, population B, which evolved toward a lower maximum, had a distribution that contained only deleterious mutants. We interpret these distributions to measure the fitness effects of genotypes that are mutationally available to the two populations. Thus, the evolvability of phi6 is constrained by the distribution of its mutational neighbours, despite the fact that this phage has the characteristic high mutation rate of RNA viruses.     

Spatial clumping of sexually receptive females induces space sharing among male voles

The spatial organization of individuals in populations (their spacing system) can be highly variable even among populations of the same species. As spacing systems have important consequences for ecological processes such as population regulation, competition and mating systems, there have been many attempts to explore factors that may cause this variation. For mammals, it has been argued that the spatial distribution of sexually receptive females is the most important factor determining the spacing system of males, whereas habitat characteristics are most important to females. This has been difficult to test experimentally as it requires manipulations of the spatial distribution of the opposite sex without changing other properties of the environment. Here, I present a novel experimental procedure that can achieve this and demonstrate that the spatial distribution of the opposite sex in a population of voles is indeed an important determinant of the spacing system of males, but not of females. However, the effects on males are different from those predicted by many theoretical studies.     

Evolution driven by differential dispersal within a wild bird population

Evolutionary theory predicts that local population divergence will depend on the balance between the diversifying effect of selection and the homogenizing effect of gene flow. However, spatial variation in the expression of genetic variation will also generate differential evolutionary responses. Furthermore, if dispersal is non-random it may actually reinforce, rather than counteract, evolutionary differentiation. Here we document the evolution of differences in body mass within a population of great tits, Parus major, inhabiting a single continuous woodland, over a 36-year period. We show that genetic variance for nestling body mass is spatially variable, that this generates different potential responses to selection, and that this diversifying effect is reinforced by non-random dispersal. Matching the patterns of variation, selection and evolution with population ecological data, we argue that the small-scale differentiation is driven by density-related differences in habitat quality affecting settlement decisions. Our data show that when gene flow is not homogeneous, evolutionary differentiation can be rapid and can occur over surprisingly small spatial scales. Our findings have important implications for questions of the scale of adaptation and speciation, and challenge the usual treatment of dispersal as a force opposing evolutionary differentiation.     

Genetic diversity among Chinese sika deer （Cerrus nippon） populations and relationships between Chinese and Japanese sika deer

Sika deer （Cervus nippon） is a cervid endemic to mainland and insular Asia and endangered. We analyzed variation in the mitochondrial DNA （mtDNA） control region for four subspecies to understand the genetic diversity, population structure and evolutionary history in China. 335 bp were sequenced and eight haplotypes were identified based on 25 variable sites among the populations. Sika deer in China showed lower genetic diversity, sug- gesting a small effective population size due to habitat fragmentation, a low number of founder individuals, or the narrow breeding program. AMOVA analysis indicated that there was significant genetic subdivision among the four populations, but no correlation between the genetic and geographic distance. PhyIogenetic analyses also revealed that Chinese sika deer may be divided into three genetic clades, but the genetic structure among Chinese populations was inconsistent with subspecies designations and present geographic distribution. Including the sequence data of Japanese sika deer, the results indicated that Chinese populations were more closely related to Southern Japanese populations than to the Northern Japanese one, and the Taiwan population was closer to populations of Northeastern China and Sichuan than to those of Southern China.