Abstract

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.

Highlights

  • Sexual selection favours traits that confer an advantage in intra-sexual competition in both sexes [1]

  • Sexual selection studies have focused on males, it is appreciated that intra-sexual competition can play an important role in the evolution of females, which in turn affect males responses to female adaptations [2, 3]

  • Large adult females mated significantly more frequently, mated with significantly more mates, and produced significantly more offspring, than small females across all experiments in which female body size was manipulated (i.e. Female Experiment and Female-Male experiment) (Table 1, Fig 2A–2F, S1 Fig)

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Summary

Introduction

Sexual selection favours traits that confer an advantage in intra-sexual competition in both sexes [1]. If so, being small could potentially reduce the benefits of multiple matings for males–in which case we would expect to observe reduced Bateman gradients–and could modulate post-copulatory competitiveness [40] Both large and small males invest more seminal fluid when mating with large females, suggesting that males can adjust their ejaculate investment depending on the body size of their mates [36]. We expected female Bateman gradients to be steeper in female mixed size social environments due to the association between body size, number of mates and offspring production Because this effect relies solely on female’s physiological and behavioural traits, we did not predict effects of male body size variation in this pattern. When manipulating both sexes body size, we expected to strengthen sexual selection on male size by enabling large males to outcompete small males over large, more fecund females and their eggs, and by enabling large females to outcompete small females over access to large males and their sperm

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