BackgroundBehavioural phenotypes vary within and among individuals. While early-life experiences have repeatedly been proposed to underpin interactions between these two hierarchical levels, the environmental factors causing such effects remain under-studied. We tested whether an individual’s diet affected both its body composition, average behaviour (thereby causing among-individual variation or ‘personality’) and within-individual variability in behaviour and body weight (thereby causing among-individual differences in residual within-individual variance or ‘stability’), using the Southern field cricket Gryllus bimaculatus as a model. We further asked whether effects of diet on the expression of these variance components were sex-specific.MethodsManipulating both juvenile and adult diet in a full factorial design, individuals were put, in each life-stage, on a diet that was either relatively high in carbohydrates or relatively high in protein. We subsequently measured the expression of multiple behavioural (exploration, aggression and mating activity) and morphological traits (body weight and lipid mass) during adulthood.ResultsDietary history affected both average phenotype and level of within-individual variability: males raised as juveniles on high-protein diets were heavier, more aggressive, more active during mating, and behaviourally less stable, than conspecifics raised on high-carbohydrate diets. Females preferred more protein in their diet compared to males, and dietary history affected average phenotype and within-individual variability in a sex-specific manner: individuals raised on high-protein diets were behaviourally less stable in their aggressiveness but this effect was only present in males. Diet also influenced individual differences in male body weight, but within-individual variance in female body weight.DiscussionThis study thereby provides experimental evidence that dietary history explains both heterogeneous residual within-individual variance (i.e., individual variation in ‘behavioural stability’) and individual differences in average behaviour (i.e., ‘personality’), though dietary effects were notably trait-specific. These findings call for future studies integrating proximate and ultimate perspectives on the role of diet in the evolution of repeatedly expressed traits, such as behaviour and body weight.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0852-4) contains supplementary material, which is available to authorized users.

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There is increasing interest in the proximate factors that underpin individual variation in suites of correlated behaviours. In this paper, we propose that dietary macronutrient composition, an underexplored environmental factor, might play a key role. Variation in macronutrient composition can lead to among-individual differentiation in single behaviours (‘personality’ ) as well as among-individual covariation between behaviours (‘behavioural syndromes’ ). Here, we argue that the nutritional balance during any life stage might affect the development of syndrome structure and the expression of genes with pleiotropic effects that influence development of multiple behaviours, hence genetic syndrome structure. We further suggest that males and females should typically differ in diet-dependent genetic syndrome structure despite a shared genetic basis. We detail how such diet-dependent multivariate gene-environment interactions can have major repercussions for the evolution of behavioural syndromes.

Empirical studies imply that sex-specific genetic architectures can resolve evolutionary conflicts between males and females, and thereby facilitate the evolution of sexual dimorphism. Sex-specificity of behavioural genetic architectures has, however, rarely been considered. Moreover, as the expression of genetic (co)variances is often environment-dependent, general inferences on sex-specific genetic architectures require estimates of quantitative genetics parameters under multiple conditions. We measured exploration and aggression in pedigreed populations of southern field crickets () raised on either naturally balanced (free-choice) or imbalanced (protein-deprived) diets. For each dietary condition, we measured for each behavioural trait (i) level of sexual dimorphism, (ii) level of sex-specificity of survival selection gradients, (iii) level of sex-specificity of additive genetic variance, and (iv) strength of the cross-sex genetic correlation. We report here evidence for sexual dimorphism in behaviour as well as sex-specificity in the expression of genetic (co)variances as predicted by theory. The additive genetic variances of exploration and aggression were significantly greater in males compared with females. Cross-sex genetic correlations were highly positive for exploration but deviating (significantly) from one for aggression; findings were consistent across dietary treatments. This suggests that genetic architectures characterize the sexually dimorphic focal behaviours across various key environmental conditions in the wild. Our finding also highlights that sexual conflict can be resolved by evolving sexually independent genetic architectures.