The gut microbiota affects a wide spectrum of host physiological traits, including development [1-5], germline [6], immunity [7-9], nutrition [4, 10, 11], and longevity [12, 13]. Association with microbes also influences fitness-related behaviors such as mating [14] and social interactions [15, 16]. Although the gut microbiota is evidently important for host wellbeing, how hosts become associated with particular assemblages of microbes from the environment remains unclear. Here, we present evidence that the gut microbiota can modify microbial and nutritional preferences of Drosophila melanogaster. By experimentally manipulating the gut microbiota of flies subjected to behavioral and chemosensory assays, we found that fly-microbe attractions are shaped by the identity of the host microbiota. Conventional flies exhibit preference for their associated Lactobacillus, a behavior also present in axenic flies as adults and marginally as larvae. By contrast, fly preference for Acetobacter is primed by early-life exposure and can override the innate preference. These microbial preferences are largely olfactory guided and have profound impact on host foraging, as flies continuously trade off between acquiring beneficial microbes and balancing nutrients from food. Our study shows a role of animal microbiota in shaping host fitness-related behavior through their chemosensory responses, opening a research theme on the interrelationships between the microbiota, host sensory perception, and behavior.

The developmental environment can potentially alter the adult social environment and influence traits targeted by sexual selection such as body size. In this study, we manipulated larval density in male and female Drosophila melanogaster, which results in distinct adult size phenotypes–high (low) densities for small (large) adults–and measured sexual selection in experimental groups consisting of adult males and females from high, low, or a mixture of low and high larval densities. Overall, large adult females (those reared at low larval density) had more matings, more mates and produced more offspring than small females (those reared at high larval density). The number of offspring produced by females was positively associated with their number of mates (i.e. there was a positive female Bateman gradient) in social groups where female size was experimentally varied, likely due to the covariance between female productivity and mating rate. For males, we found evidence that the larval environment affected the relative importance of sexual selection via mate number (Bateman gradients), mate productivity, paternity share, and their covariances. Mate number and mate productivity were significantly reduced for small males in social environments where males were of mixed sizes, versus social environments where all males were small, suggesting that social heterogeneity altered selection on this subset of males. Males are commonly assumed to benefit from mating with large females, but in contrast to expectations we found that in groups where both the male and female size varied, males did not gain more offspring per mating with large females. Collectively, our results indicate sex-specific effects of the developmental environment on the operation of sexual selection, via both the phenotype of individuals, and the phenotype of their competitors and mates.

Population density modulates a wide range of eco-evolutionary processes including inter- and intra-specific competition, fitness and population dynamics. In holometabolous insects, the larval stage is particularly susceptible to density-dependent effects because the larva is the resource-acquiring stage. Larval density-dependent effects can modulate the expression of life-history traits not only in the larval and adult stages but also downstream for population dynamics and evolution. Better understanding the scope and generality of density-dependent effects on life-history traits of current and future generations can provide useful knowledge for both theory and experiments in developmental ecology. Here, we review the literature on larval density-dependent effects on fitness of non-social holometabolous insects. First, we provide a functional definition of density to navigate the terminology in the literature. We then classify the biological levels upon which larval density-dependent effects can be observed followed by a review of the literature produced over the past decades across major non-social holometabolous groups. Next, we argue that host-microbe interactions are yet an overlooked biological level susceptible to density-dependent effects and propose a conceptual model to explain how density-dependent effects on host-microbe interactions can modulate density-dependent fitness curves. In summary, this review provides an integrative framework of density-dependent effects across biological levels which can be used to guide future research in the field of ecology and evolution.

Developmental conditions can strongly influence adult phenotypes and social interactions, which in turn affect key evolutionary processes such as sexual selection and sexual conflict. While the implications of social interactions in phenotypically mixed populations at the individual level are increasingly well known, how these effects influence the fate of groups remains poorly understood, which limits our understanding of the broader ecological implications. To address this problem we manipulated adult phenotypes and social composition in Drosophila melanogaster – by experimentally manipulating the larval density of the group-members – and measured a range of group-level outcomes across the lifespan of groups. Adult groups composed of exclusively low larval-density individuals showed high courtship levels, and low early reproductive rates, group growth rates, offspring mass and offspring eclosion success, relative to high larval-density or mixed larval-density groups. Furthermore, high larval-density groups had lower survival. Offspring mass increased with time, but at a reduced rate in groups when male group members (but not females) were from a mixture of larval-densities; peak reproductive rates were also earlier in these groups. Our results suggest that that variation in developmental conditions experienced by adult group members can modify the reproductive output of groups.