Abstract

Sexual reproduction is a complex process that contributes to differences between the sexes and divergence between species. From a male's perspective, sexual selection can optimize reproductive success by acting on the variance in mating success (pre-insemination selection) as well as the variance in fertilization success (post-insemination selection). The balance between pre- and post-insemination selection has not yet been investigated using a strong hypothesis-testing framework that directly quantifies the effects of post-insemination selection on the evolution of reproductive success. Here we use experimental evolution of a uniquely engineered genetic system that allows sperm production to be turned off and on in obligate male-female populations of Caenorhabditis elegans. We show that enhanced post-insemination competition increases the efficacy of selection and surpasses pre-insemination sexual selection in driving a polygenic response in male reproductive success. We find that after 10 selective events occurring over 30 generations post-insemination selection increased male reproductive success by an average of 5- to 7-fold. Contrary to expectation, enhanced pre-insemination competition hindered selection and slowed the rate of evolution. Furthermore, we found that post-insemination selection resulted in a strong polygenic response at the whole-genome level. Our results demonstrate that post-insemination sexual selection plays a critical role in the rapid optimization of male reproductive fitness. Therefore, explicit consideration should be given to post-insemination dynamics when considering the population effects of sexual selection.

Highlights

  • Sexual selection drives the evolution of some of the most remarkable phenotypes observed in nature

  • Our results demonstrate that post-insemination sexual selection plays a critical role in the rapid optimization of male reproductive fitness

  • Some of the most dramatic and diverse phenotypes observed in nature––such as headbutting in wild sheep and the elaborate tails of peacocks––are sexually dimorphic. These remarkable phenotypes are a result of sexual selection optimizing reproductive success in females and males independently

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Summary

Introduction

Sexual selection drives the evolution of some of the most remarkable phenotypes observed in nature. Sexual selection has the potential to act on both the variance in mating success and the variance in fertilization success ( referred to as gametic selection [2,3]). Whether selection during these reproductive phases interacts in an additive, antagonistic, or synergistic manner to optimize total male reproductive success is understudied. Understanding this balance is critical for understanding how sexual selection shapes the evolution of reproductive success over time. Such processes are critical for relating the role of sexual selection to population adaptation [4,5] and divergence [6]

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