The evolution of social monogamy in mammals.

The evolution of social monogamy has intrigued biologists for over a century. Here, we show that the ancestral condition for all mammalian groups is of solitary individuals and that social monogamy is derived almost exclusively from this social system. The evolution of social monogamy does not appear to have been associated with a high risk of male infanticide, and paternal care is a consequence rather than a cause of social monogamy. Social monogamy has evolved in nonhuman mammals where breeding females are intolerant of each other and female density is low, suggesting that it represents a mating strategy that has developed where males are unable to defend access to multiple females.The Leverhulme Trust, the Isaac Newton Trust, and the European Research Council provided the funding for this study.This version is the author accepted manuscript. The final published version can be found here: http://www.sciencemag.org/content/341/6145/526.ful

Endocranial volume is heritable and is associated with longevity and fitness in a wild mammal

Research on relative brain size in mammals suggests that increases in brain size may generate benefits to survival and costs to fecundity: comparative studies of mammals have shown that interspecific differences in relative brain size are positively correlated with longevity and negatively with fecundity. However, as yet, no studies of mammals have investigated whether similar relationships exist within species, nor whether individual differences in brain size within a wild population are heritable. Here we show that, in a wild population of red deer ($\textit{Cervus elaphus}$), relative endocranial volume was heritable (h² = 63%; 95% credible intervals (CI) = 50-76%). In females, it was positively correlated with longevity and lifetime reproductive success, though there was no evidence that it was associated with fecundity. In males, endocranial volume was not related to longevity, lifetime breeding success or fecundity.Leverhulme Trust; Isaac Newton Trust; Natural Environmental Research Council (NE/L00688X/1); European Research Council (grant nos. 250098 and 294494); Australian Research Counci

Pregnancy is detected via odour in a wild cooperative breeder

Among mammals, scent has long been known to encode oestrus, however in many species detecting pregnancy may also be important in terms of both competition and mate-choice. Here we show, through odour presentation experiments, that pregnancy is discernible via scent by both sexes in the cooperatively breeding banded mongoose. Males spent more time investigating and were more likely to scent mark the odours of non-pregnant females, compared to pregnant females. Females showed increased levels of scent marking when odours were of the same reproductive state as themselves. These results present the first direct demonstration that pregnancy is detectable via scent in wild cooperative breeders. Detecting pregnancy may be particularly important in cooperative breeders as, in addition to the competition between males for receptive mates, there is also intense competition between females for access to alloparental care. Consequently, dominant females benefit from targeting reproductive suppression towards subordinates that represent direct threats, such as pregnant females

Multiple pathways mediate the effects of climate change on maternal reproductive traits in a red deer population

Temporal changes in phenological traits arising as a consequence of recent rapid environmental change have been widely demonstrated in animal populations. Increasingly, studies are seeking to understand the impact of changes in such traits on individual fitness and population dynamics, with the ultimate aim of predicting population persistence or extinction under different climate scenarios. Here, we examined the effects of environmental change on maternal reproductive traits in a wild population of red deer (Cervus elaphus) and sought to explain why, despite a rapid advance in offspring birth dates, we observed no apparent consequences for offspring fitness. By using path analysis, we identified both direct and indirect paths along which changes in environmental conditions affected birth date, birth mass, juvenile survival, and female fecundity. In general, warmer temperatures were associated with earlier birth dates and greater birth mass, and higher rainfall was associated with reduced juvenile survival and reduced female fecundity. We also examined concurrent effects of population density, maternal age, and reproductive history, and found that temporal stasis in average trait values, at least in part, could be explained by antagonistic roles of direct and indirect effects of changing climate and increasing population density. Identification of the many mechanisms that contribute to the dynamics of phenotypic traits is challenging; this study demonstrates the need to consider both climatic and demographic variation in order to understand the fitness consequences of changes in phenological traits. Read More: http://www.esajournals.org/doi/abs/10.1890/13-0967.

Contrasts in kinship structure in mammalian societies

Comparative studies of mammals confirm Hamilton’s prediction that differences in cooperative and competitive behavior across species will be related to contrasts in kinship between group members. Although theoretical models have explored the factors affecting kinship within social groups, few have analyzed the causes of contrasts in kinship among related species. Here, we describe interspecific differences in average kinship between group members among social mammals and show that a simple mathematical model that includes the number of breeding females, male reproductive skew, and litter size successfully predicts ~95% of observed variation in average kinship between group members across a sample of mammals. Our model shows that a wide range of conditions can generate groups with low average relatedness but only a small and rather specific set of conditions are likely to generate high average levels of relatedness between their members, providing insight into the relative rarity of advanced forms of cooperation in mammalian societies

Maternal longevity and offspring sex in wild ungulates

In species with sexual size dimorphism, the offspring of the larger sex usually have greater energy requirements and may lead to greater fitness costs for parents. The effects of offspring sex on maternal longevity, however, have only been tested in humans. Human studies produced mixed results and considerable debate mainly owing to the difficulty of distinguishing the effects of sexual dimorphism from sociocultural factors. To advance this debate, we examined how the relative number of sons influenced maternal longevity in four species of free-living ungulates (Soay sheep Ovis aries ; bighorn sheep, Ovis canadensis ; red deer, Cervus elaphus ; mountain goat, Oreamnos americanus ), with high male-biased sexual size dimorphism but without complicating sociocultural variables. We found no evidence for a higher cumulative cost of sons than of daughters on maternal longevity. For a given number of offspring, most females with many sons in all four populations lived longer than females with few sons. The higher cost of sons over daughters on maternal lifespan reported by some human studies may be the exception rather than the rule in long-lived iteroparous species

A unified-models analysis of the development of sexual size dimorphism in Damaraland mole-rats, Fukomys damarensis

AbstractIndividual variation in growth rates often generates variation in fitness. However, the ability to draw meaningful inferences from growth data depends on the use of growth models that allow for direct comparisons of growth between the sexes, between populations, and between species. Unlike traditional sigmoid functions, a recently parameterized family of unified growth models provides a reliable basis for comparisons since each parameter affects a single curve characteristic and parameters are directly comparable across the unified family. Here, we use the unified-models approach to examine the development of sexual size dimorphism in Damaraland mole-rats (Fukomys damarensis), where breeding males are larger than breeding females. Using skeletal measurements, we show here that the larger size of male Damaraland mole-rats arises from an increased growth rate across the entire period of development, rather than through sex differences in the duration or timing of growth. Male-biased skeletal size dimorphism is not unusual among rodents, and our measures of sex differences in size in captive mole-rats are close to sexual size differences in the wild, where size dimorphism = 1.04 (male:female). We hope our study will encourage the wide use of unified growth models by mammalogists.</jats:p

Environmental coupling of selection and heritability limits evolution

There has recently been great interest in applying theoretical quantitative genetic models to empirical studies of evolution in wild populations. However, while classical models assume environmental constancy, most natural populations exist in variable environments. Here, we applied a novel analytical technique to a long-term study of birthweight in wild sheep and examined, for the first time, how variation in environmental quality simultaneously influences the strength of natural selection and the genetic basis of trait variability. In addition to demonstrating that selection and genetic variance vary dramatically across environments, our results show that environmental heterogeneity induces a negative correlation between these two parameters. Harsh environmental conditions were associated with strong selection for increased birthweight but low genetic variance, and vice versa. Consequently, the potential for microevolution in this population is constrained by either a lack of heritable variation ( in poor environments) or by a reduced strength of selection ( in good environments). More generally, environmental dependence of this nature may act to limit rates of evolution, maintain genetic variance, and favour phenotypic stasis in many natural systems. Assumptions of environmental constancy are likely to be violated in natural systems, and failure to acknowledge this may generate highly misleading expectations for phenotypic microevolution

Social complexity and kinship in animal societies

Studies of eusocial invertebrates regard complex societies as those where there is a clear division of labour and extensive cooperation between breeders and helpers. In contrast, studies of social mammals identify complex societies as those where differentiated social relationships influence access to resources and reproductive opportunities. We show here that, while traits associated with social complexity of the first kind occur in social mammals that live in groups composed of close relatives, traits associated with the complexity of social relationships occur where average kinship between female group members is low. These differences in the form of social complexity appear to be associated with variation in brain size and probably reflect contrasts in the extent of conflicts of interest between group members. Our results emphasise the limitations of any unitary concept of social complexity and show that variation in average kinship between group members has far‐reaching consequences for animal societies.This project was funded by the European Research Commission (grant no. 294494‐THCB2011)

The emergence of reciprocally beneficial cooperation

We offer a new and robust model of the emergence and persistence of cooperation when interactions are anonymous, the population is well-mixed, and evolution selects strategies according to material payoffs. The model has a Prisoner’s Dilemma structure, but with an outside option of non-participation. The payoff to mutual cooperation is stochastic; with positive probability, it exceeds that from cheating against a cooperator. Under mild conditions, mutually beneficial cooperation occurs in equilibrium. This is possible because the non-participation option holds down the equilibrium frequency of cheating. Dynamic properties of the model are investigated theoretically and through simulations based on replicator dynamics