Male mate choice influences female promiscuity in Soay sheep.

In most animal species, males are predicted to compete for reproductive opportunities, while females are expected to choose between potential mates. However, when males' rate of reproduction is constrained, or females vary widely in 'quality', male mate choice is also predicted to occur. Such conditions exist in the promiscuous mating system of feral Soay sheep on St Kilda, Scotland, where a highly synchronized mating season, intense sperm competition and limitations on sperm production constrain males' potential reproductive rate, and females vary substantially in their ability to produce successful offspring. We show that, consistent with predictions, competitive rams focus their mating activity and siring success towards heavier females with higher inclusive fitness. To our knowledge, this is the first time that male mate choice has been identified and shown to lead to assortative patterns of parentage in a natural mammalian system, and occurs despite fierce male-male competition for mates. An additional consequence of assortative mating in this population is that lighter females experience a series of unstable consorts with less adept rams, and hence are mated by a greater number of males during their oestrus. We have thus also identified a novel male-driven mechanism that generates variation in female promiscuity, which suggests that the high levels of female promiscuity in this system are not part of an adaptive female tactic to intensify post-copulatory competition between males.

Fluctuating trade-offs favour precocial maturity in male Soay sheep.

Although trade-offs between reproductive effort and survival are commonly proposed, empirical studies that quantify the true costs and benefits of breeding activity are rare. This information is crucial, however, for examining the adaptive value of important life history traits such as age at maturity. Here we estimate both the survival cost, and genetic benefits, of precocial male maturity in a highly polygynous naturally limited population of Soay sheep. While we demonstrate that early reproduction does indeed carry a survival cost, we find that young males also achieve unexpectedly high reproductive success and that precocial mating is favoured due to the fluctuating demographic structure of the population.

Soay rams target reproductive activity towards promiscuous females' optimal insemination period.

Female promiscuity is thought to have resulted in the evolution of male behaviours that confer advantages in the sperm competition that ensues. In mammalian species, males can gain a post-copulatory advantage in this sperm 'raffle' by inseminating females at the optimal time relative to ovulation, leading to the prediction that males should preferentially associate and copulate with females at these times. To the best of our knowledge, we provide the first high-resolution test of this prediction using feral Soay sheep, which have a mating system characterized by male competition for access to highly promiscuous females. We find that competitive males time their mate guarding (and hence copulations) to occur close to the optimal insemination period (OIP), when females are also increasingly likely to 'cooperate' with copulation attempts. Subordinate males practice an alternative mating tactic, where they break the integrity of the consort pair and force copulations on females. The timing of these forced copulations is also targeted towards the OIP. We thus provide quantitative evidence that female promiscuity has resulted in the evolution of reproductive strategies in which males 'load' the sperm raffle by targeting their mating activity towards female OIPs, when the probability of sperm-competition success is at its greatest.

Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success.

Male contests for access to receptive females are thought to have selected for the larger male body size and conspicuous weaponry frequently observed in mammalian species. However, when females copulate with multiple males within an oestrus, male reproductive success is a function of both pre- and postcopulatory strategies. The relative importance of these overt and covert forms of sexual competition has rarely been assessed in wild populations. The Soay sheep mating system is characterized by male contests for mating opportunities and high female promiscuity. We find that greater horn length, body size and good condition each independently influence a male's ability to monopolize receptive females. For males with large horns at least, this behavioural success translates into greater siring success. Consistent with sperm-competition theory, we also find that larger testes are independently associated with both higher copulation rates and increased siring success. This advantage of larger testes emerges, and strengthens, as the number of oestrous females increases, as dominant males can no longer control access to them all. Our results thus provide direct quantitative evidence that male reproductive success in wild populations of mammals is dependent upon the relative magnitude of both overt contest competition and covert sperm competition.

Density-dependent selection in a fluctuating ungulate population.

Despite considerable theoretical interest no direct examples of density-dependent natural selection acting on simple polymorphic variation have been documented in a natural population. Here we show that the magnitude of selective differences in survival between phenotypes in two conspicuous polymorphisms of coat colour and horn type in Soay sheep Ovis aries living on St Kilda, Scotland are associated with marked changes in population density. Selection is strongest in years of high density but weak in years of low density. In addition to direct observations of density-dependent 'soft' selection in a natural population, the analysis revealed that the level of overcompensatory mortality (responsible for promoting population instability) was higher after accounting for genetic variation in the coat and horn morph traits. The results emphasize the importance of understanding the interaction between selection and population demography for both genetic and ecological studies of natural populations.

Density-dependent selection on horn phenotype in Soay sheep.

In the naturally regulated population of Soay sheep (Ovis aries L.) on Hirta (St Kilda), 12% of males and 24% of females have scurred horns. This trait reduces the competitive ability of males in the mating season but is associated with higher overwinter survival rates in both sexes (Moorcroft et al. 1996). In this paper, we show that scurred females also show higher conception rates and weaning rates than non-scurred ones, and that these differences are associated with heavier maternal body weight as well as higher birth weights of offspring. Selection pressures favouring scurredness in females vary with population density and are generally more pronounced among younger animals than adults. We discuss these results with reference to recent suggestions that temporal fluctuation in selection pressures may help to maintain genetic diversity within populations. We suggest that selection against scurredness operating through male mating success is opposed by selection favouring this trait, operating through the breeding success of females and the survival of both sexes.

State-dependent life history evolution in Soay sheep: dynamic modelling of reproductive scheduling.

Adaptive decisions concerning the scheduling of reproduction in an animal's lifetime, including age at maturity and clutch or litter size, should depend on an animal's body condition or state. In this state-dependent case, we are concerned with the optimization of sequences of actions and so dynamic optimization techniques are appropriate. Here we show how stochastic dynamic programming can be used to study the reproductive strategies and population dynamics of natural populations, assuming optimal decisions. As examples we describe models based upon field data from an island population of Soay sheep on St. Kilda. This population shows persistent instability, with cycles culminating in high mortality every three or four years. We explore different assumptions about the extent to which Soay ewes use information about the population cycle in making adaptive decisions. We compare the observed distributions of strategies and population dynamics with model predictions; the results indicate that Soay ewes make optimal reproductive decisions given that they have no information about the population cycle. This study represents the first use of a dynamic optimization life history model of realistic complexity in the study of a field population. The techniques we use are potentially applicable to many other populations, and we discuss their extension to other species and other life history questions.

Molecular genetic variation and individual survival during population crashes of an unmanaged ungulate population.

Theoretical models of the effect of population bottlenecks on genetic variation assume that individuals are removed at random from the population. We investigated this assumption in a naturally regulated, unstable population of Soay sheep (Ovis aries). During rapid population declines or 'crashes', individuals were not removed at random with respect to genotype: we found associations between individual survival and certain genotypes at five polymorphic protein or microsatellite DNA loci (Ada, Got, Tf, MAF18 and OPACAP). Some loci appeared to show simple associations with survival whereas others had more complex interactions with crash year or age: all displayed different patterns of association between the sexes. Simple overdominance was not a general feature of our data; it seems likely that fluctuating selecting, countervailing selection in different fitness components or frequency-dependent selection may explain the pattern and complexity of the associations shown at different loci. Our study cannot distinguish between selection acting at these loci or at other, closely linked loci. However, our empirical study implies that the molecular genetic outcome of population bottlenecks in natural populations does not always follow theoretical expectations based on the random removal of genotypes. Bottlenecks in which individuals are removed at random are distinct from bottlenecks in which there is scope for selection via non-random survival of individuals.