How is behaviour constrained within typical sex roles?

Sex differences in behaviour are ubiquitous among sexually reproducing animals. In vertebrates such as mammals, males typically devote conspicuous effort to competing for mates but show little or no parental care, whereas females often show high levels of parental care but invest less conspicuous effort in competing for beneficial resources. Why don't males invest more in parental care and females invest more in competition? Explaining how and why these differences have evolved is more than an interesting question in its own right. It is also a key component in the bigger puzzle of explaining the evolution of biological diversity. Consequently, theory of very broad significance has been developed to explain how typical sex roles evolve. We know that key sex differences are rooted in anisogamy (the production of sperm and eggs), and amplified by sexual selection (competition for mates and fertilisations). This can explain why females are typically the more caring sex and males more often compete for mates, but doesn't preclude males from caring for offspring, or females from competing aggressively for resources. A key question is therefore whether competition (for mates by males, and resources by females) limits the ability to invest in parental care. If so, male care may be constrained because it limits mating success, and female competitive behaviour constrained because it limits parental care. Rigorous tests of these ideas have proved elusive however, since classical approaches, based on comparisons between different species, cannot resolve the essential mechanistic elements of hypothesised constraints on the behaviour of each sex. We propose to achieve this by exploiting continuous variation within typical sex roles of a model vertebrate, the wild house mouse. The house mouse is a highly tractable experimental subject that is especially amenable to genome-level analysis, with the added advantage that a great deal is already known about the genetics and neurobiology of its behaviour from laboratory mice. This offers an exceptional opportunity for the application of powerful new advances in next generation sequencing to test the underlying mechanisms by which competition affects parental care. Typical of polygynous vertebrates, male house mice invest strongly in competing for mates, but our latest research also reveals that they show varying levels of parental care. Similarly, female house mice invest strongly in parental care, but also show varying levels of costly competitive behaviours. We will utilise this natural variation within typical sex roles to explore the factors that constrain caring behaviours by competitive males and competitive behaviours by caring females. We will use an experimental approach, manipulating social environments under carefully controlled naturalistic conditions to: 1) quantify how increased investment in competition affects parental behaviours in either sex, according to competitive phenotype, and 2) assess how parental responses to competition are mediated in either sex, to test for evidence of predicted physiological constraints on behaviour, and trade-offs with costly competitive signalling. We will also utilise behavioural variation to compare genome-wide gene expression patterns, determining: 3) if a high level of parental care by males is associated with 'de-masculinisation' of gene expression, constraining the ability to successfully compete, and 4) if a high level of competitive behaviour by females is associated with 'de-feminisation' of gene expression, constraining the ability to successfully care for young. Our overall approach will thus provide a uniquely comprehensive analysis of how intrasexual competition leads to divergent sex-typical behaviours. By testing mechanistic constraints on behaviour within typical sex roles, our research programme promises to unlock new answers to a fundamental evolutionary question, with broad implications for understanding biological diversity.

The proposed research has fundamental implications for understanding variation in the social behaviour of vertebrate animals. This offers broad potential economical and societal impacts over both short and long timescales. Understanding the factors that facilitate parental care or trigger aggression is of particular significance for those who manage animals, whether wild, laboratory or livestock - for example those managing or breeding endangered animals for conservation purposes (conservationists, zoological curators), using animals in research and testing (animal care staff, researchers), and associated regulators and animal welfare advisors (Home office inspectorate, NC3Rs, RSPCA, UFAW); and those involved with the farming industry (farmers, veterinary surgeons, animal breeding industry).

Understanding social and environmental influences on parental care and aggression has broad relevance for: i) captive management and breeding of wild animals for conservation; ii) welfare of laboratory animals; iii) better understanding of unexplained variation among laboratory mice (e.g. in biomedical research) where the influences of social grouping on females are largely unknown; iv) management and breeding of livestock where there are problems in maintaining high reproductive performance and welfare; v) animal models of social cognition and behaviour used in biomedical research. Understanding how female fertility might be constrained by social conditions is also important to breeding success of managed animals in each of these contexts. For natural populations, there is a potential impact for our research in predicting the impact of increased competition between females on parental care as resources and space become increasingly constrained in fragmented habitats, and the environmental impact of steroidal oestrogens and their effects on reproductive traits. The biological basis of sex differences in behaviour is also likely to be of wide interest to the general public and school children studying fundamental aspects of animal behaviour. Sex differences are a particularly topical area in relation to human behaviour, widely popularized as a subject of popular science books and journalism.