Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster

Bahar Patlar,Alberto Civetta

doi:10.1186/s12862-022-01975-1

Abstract

BackgroundThe rapid evolution of seminal fluid proteins (SFPs) has been suggested to be driven by adaptations to postcopulatory sexual selection (e.g. sperm competition). However, we have recently shown that most SFPs evolve rapidly under relaxed selective pressures. Given the role of SFPs in competition for fertilization phenotypes, like the ability to transfer and store sperm and the modulation of female receptivity and ovulation, the prevalence of selectively relaxed SFPs appears as a conundrum. One possible explanation is that selection on SFPs might be relaxed in terms of protein amino acid content, but adjustments of expression are essential for post-mating function. Interestingly, there is a general lack of systematic implementation of gene expression perturbation assays to monitor their effect on phenotypes related to sperm competition.ResultsWe successfully manipulated the expression of 16 SFP encoding genes using tissue-specific knockdowns (KDs) and determined the effect of these genes’ perturbation on three important post-mating phenotypes: female refractoriness to remating, defensive (P1), and offensive (P2) sperm competitive abilities in Drosophila melanogaster. Our analyses show that KDs of tested SFP genes do not affect female refractoriness to remating and P2, however, most gene KDs significantly decreased P1. Moreover, KDs of SFP genes that are selectively constrained in terms of protein-coding sequence evolution have lower P1 than KDs of genes evolving under relaxed selection.ConclusionsOur results suggest a more predominant role, than previously acknowledged, of variation in gene expression than coding sequence changes on sperm competitive ability in D. melanogaster.

Highlights

The rapid evolution of seminal fluid proteins (SFPs) has been suggested to be driven by adaptations to postcopulatory sexual selection
A second possibility is that several SFPs are selectively relaxed because amino acid changes do not cause any modification of protein function, but changes in expression and the amount of product are essential for gene function and subjected to selective pressures
RNAi knockdowns We tested the effectiveness of knockdowns by using qPCR to measure the expression of target genes (Table 1) in knockdown flies relative to wild-type controls

Summary

Introduction

The rapid evolution of seminal fluid proteins (SFPs) has been suggested to be driven by adaptations to postcopulatory sexual selection (e.g. sperm competition). Seminal fluid proteins (SFPs) are recognized to be among those evolving the fastest [1, 4,5,6,7,8] Both population genetics and molecular evolution studies have found a limited number of SFPs under positive directional selection [4, 7, 9, 10]. One possibility is that a limited number of SFPs under positive or purifying selection are sufficient to drive adaptations at the phenotypic level This is likely to take place under a genetic architecture in which a handful of major genes exert main effects, with modulation by minor modifiers [20]. If changes in expression of SFP genes affect male fitness, understanding the effect of gene expression perturbation on fitness shall offer a better opportunity to establish links between the evolution of genotypes and phenotypes

Methods

Results

Conclusion