Sexual selection can partly explain low frequencies of Segregation Distorter alleles.

Thomas A Keaney,Luke Holman,Therésa M Jones

doi:10.1098/rspb.2021.1190

Abstract

The Segregation Distorter (SD) allele found in Drosophila melanogaster distorts Mendelian inheritance in heterozygous males by causing developmental failure of non-SD spermatids, such that greater than 90% of the surviving sperm carry SD. This within-individual advantage should cause SD to fix, and yet SD is typically rare in wild populations. Here, we explore whether this paradox can be resolved by sexual selection, by testing if males carrying three different variants of SD suffer reduced pre- or post-copulatory reproductive success. We find that males carrying the SD allele are just as successful at securing matings as control males, but that one SD variant (SD-5) reduces sperm competitive ability and increases the likelihood of female remating. We then used these results to inform a theoretical model; we found that sexual selection could limit SD to natural frequencies when sperm competitive ability and female remating rate equalled the values observed for SD-5. However, sexual selection was unable to explain natural frequencies of the SD allele when the model was parameterized with the values found for two other SD variants, indicating that sexual selection alone is unlikely to explain the rarity of SD.

Highlights

In sexually-reproducing organisms, meiosis ensures that autosomal alleles are divided evenly between the haploid gametes
Segregation Distorter (SD) variant (SD-5) reduces sperm competitive ability and increases the likelihood of female remating. We used these results to inform a theoretical model; we found that sexual selection could limit SD to natural frequencies when sperm competitive ability and female remating rate equalled the values observed for SD-5
We evaluated whether sexual selection might explain the observed low allele frequencies of the SD selfish allele, using experiments and a model

Summary

Introduction

In sexually-reproducing organisms, meiosis ensures that autosomal alleles are divided evenly between the haploid gametes This equitable transmission can be subverted by ‘selfish genetic elements’ which encode phenotypes that are selected to increase their own propagation, at the expense of other alleles in the genome [1]. These selfish alleles have manifold ecological and evolutionary consequences [2], and given their potential to spread even when they lower the fitness of individuals carrying them, efforts are underway to develop synthetic selfish alleles that mimic their effects, with the aim to modify or suppress populations [3]. The result is that >90% of the male’s functional sperm carry SD, rather than the 50% expected for a typical heterozygous locus [6]

Methods

Results

Conclusion