Direct and indirect effects of male genital elaboration in female seed beetles.

Göran Arnqvist,Karl Grieshop,Michal Polak,Locke Rowe,Johanna Rönn,Cosima Hotzy

doi:10.1098/rspb.2021.1068

Abstract

Our understanding of coevolution between male genitalia and female traits remains incomplete. This is perhaps especially true for genital traits that cause internal injuries in females, such as the spiny genitalia of seed beetles where males with relatively long spines enjoy a high relative fertilization success. We report on a new set of experiments, based on extant selection lines, aimed at assessing the effects of long male spines on females in Callosobruchus maculatus. We first draw on an earlier study using microscale laser surgery, and demonstrate that genital spines have a direct negative (sexually antagonistic) effect on female fecundity. We then ask whether artificial selection for long versus short spines resulted in direct or indirect effects on female lifetime offspring production. Reference females mating with males from long-spine lines had higher offspring production, presumably due to an elevated allocation in males to those ejaculate components that are beneficial to females. Remarkably, selection for long male genital spines also resulted in an evolutionary increase in female offspring production as a correlated response. Our findings thus suggest that female traits that affect their response to male spines are both under direct selection to minimize harm but are also under indirect selection (a good genes effect), consistent with the evolution of mating and fertilization biases being affected by several simultaneous processes.

Highlights

Our understanding of the evolution of reproductive traits through sexual selection is comprehensive [1,2], some aspects of this process remain unresolved
The second assay showed that selection on male spine length significantly affected female fitness as a correlated response: females derived from L lines showed a 6% elevation in lifetime offspring production compared to females from S lines, averaged over all mates, demonstrating a positive genetic covariance between male genital morphology and female lifetime offspring production
Our experiments on a well-known model system of sexually antagonistic coevolution reveal a surprisingly complex economy of costs and benefits to females of injurious male genitalia. These include direct costs and direct benefits and, surprisingly, indirect benefits associated with the evolutionary elaboration of genitalia in males

Summary

Introduction

Our understanding of the evolution of reproductive traits through sexual selection is comprehensive [1,2], some aspects of this process remain unresolved. Male traits may reflect the genetic quality of their bearer, which in turn opens up the possibility of good genes effects [18,22,23] At this stage, females mating to males with exaggerated antagonistic traits may gain indirect benefits through the production of offspring sired by high genetic quality fathers. Comparative studies within [25,27] and across [26] species have provided support for such costs and for sexually antagonistic coevolution It is, very difficult to assess the cost of spines to female fitness due to the confounding effects of both female resistance adaptations and male traits that both covary with genital spines [37]. Males with long and short evolved spines were used to study the effects on the economics of female reproduction

Methods

Results

Findings

Discussion