Spatial environmental complexity mediates sexual conflict and sexual selection in Drosophila melanogaster.

Heather L Malek,Tristan A F Long

doi:10.1002/ece3.4932

Abstract

Sexual selection is an important agent of evolutionary change, but the strength and direction of selection often vary over space and time. One potential source of heterogeneity may lie in the opportunity for male–male and/or male–female interactions imposed by the spatial environment. It has been suggested that increased spatial complexity permits sexual selection to act in a complementary fashion with natural selection (hastening the loss of deleterious alleles and/or promoting the spread of beneficial alleles) via two (not mutually exclusive) pathways. In the first scenario, sexual selection potentially acts more strongly on males in complex environments, allowing males of greater genetic “quality” a greater chance of outcompeting rivals, with benefits manifested indirectly in offspring. In the second scenario, increased spatial complexity reduces opportunities for males to antagonistically harm females, allowing females (especially those of greater potential fecundities) to achieve greater reproductive success (direct fitness benefits). Here, using Drosophila melanogaster, we explore the importance of these mechanisms by measuring direct and indirect fitness of females housed in simple vial environments or in vials in which spatial complexity has been increased. We find strong evidence in favor of the female conflict‐mediated pathway as individuals in complex environments remated less frequently and produced more offspring than those housed in a simpler spatial environment, but no difference in the fitness of sons or daughters. We discuss these results in the context of other recent studies and what they mean for our understanding of how sexual selection operates.

Highlights

Patterns of nonrandom mating that arise as a consequence of either intra‐ or intersexual selection can have potentially dramatic consequences for a species’ evolutionary trajectory
We set out to examine how changes in spatial complexity potentially alter the outcome of mating dynamics in Drosophila melanogaster, a model species for the study of sexual selection and conflict
We show that in D. melanogaster—an important model species for the study of sexual conflict and sexual selection—that an increase in environmental spatial complexity is associated with substantially increased offspring production in females, but had apparently no significant indirect genetic benefits that could be detected in the generation

Summary

| INTRODUCTION

Patterns of nonrandom mating that arise as a consequence of either intra‐ or intersexual selection can have potentially dramatic consequences for a species’ evolutionary trajectory. In a short‐term assay conducted using D. melanogaster males placed in two vastly different sized environments, MacLellan, Whitlock, and Rundle (2009) found that the strength of sexual selection acting against males possessing visible mutations (with potentially deleterious effects) was greater in larger chambers, presumably due to the increased search effort required to find females As this assay ran for only 24 hr and most females mated only once, most of this variation was attributed to searching efficiency and precopulatory traits, rather than traits involved in pre‐ or postcopulatory male–male contest competition (or female choice, for that matter). We set out to conduct such empirical studies by exploring male–female interactions in D. melanogaster with specific attention paid to their role in mediating male‐induced harm and remating rates, and how these both potentially contribute to the fitness of offspring in the generation

| MATERIALS AND METHODS

Findings

| DISCUSSION