Female genetic contributions to sperm competition in Drosophila melanogaster

Abstract

In many species, sperm can remain viable in the reproductive tract of a female well beyond the typical interval to remating. This creates an opportunity for sperm from different males to compete for oocyte fertilization inside the female's reproductive tract.In Drosophila melanogaster, sperm morphology and seminal fluid content affect male success in sperm competition. On the other hand, although genome-wide association studies (GWAS) have demonstrated that female genotype plays a role in sperm competition outcome as well, the biochemical, sensory and physiological processes by which females detect and selectively use sperm from different males remain elusive.Here, we functionally tested 27 candidate genes implicated via a GWAS for their contribution to the female's role in sperm competition, measured as changes in the relative success of the first male to mate (P1). Of these 27 candidates, we identified eight genes that affect P1 when knocked down in females, and also showed that six of them do so when knocked down in the female nervous system. Two genes in particular, Rim and caup, lowered P1 when knocked down in sensory pickpocket (ppk) + neurons and octopaminergic Tdc2 + neurons, respectively. These results establish a functional role for the female's nervous system in the process of sperm competition and expand our understanding of the genetic, neuronal and mechanistic basis of female responses to multiple matings. We propose that through their nervous system, females actively assess male compatibility based on courtship or ejaculates and modulate sperm competition outcome accordingly.

How female × male and male × male interactions influence competitive fertilization inDrosophila melanogaster

“…2013; Ala‐Honkola and Manier 2016; Chen et al. 2019), and interactive effects between the sexes and competing males (Clark et al. 1999; Mack et al.…”

Gamete-level immunogenetic incompatibility in humans–towards deeper understanding of fertilization and infertility?

“…Despite the potential relevance of such nonrandom gamete-level interactions both from evolutionary and clinical point of view, the molecular-level mechanisms of gamete-mediated mate choice have remained largely unclear (but see Kekäläinen and Evans 2017;Chen et al 2019). Ejaculates are known to trigger a strong immune response in the reproductive tract of the females, and the strength of the response shows considerable individual variation across human males (Sharkey et al 2007).…”

Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster

“…3 Female refractoriness to remating. The percentage of females that remated with a GFP reference males within 3 days after their first mating with experimental KDs (grey lines) or wild-type control (red line) males reported as having low but detectable expression in the female brain (FlyAtlas2) and it is known that females can influence sperm utilization and both offense and defence sperm competition outcomes [31,[41][42][43].…”

“…Only eight KDs (Acp29AB, Acp53Ea, aqrs, CG11598, CG34002, CG9168, Qsox4, and Sems) had significant short-term (vial 2) decline in P1 (Additional file 1: Table S3). Temporal effects of KDs on sperm competitiveness (P1 and P2) have been previously reported [31,32]. Differences in P1 between males can result from variation in the ability of first to mate males to interfere with the sperm from an incoming second male (e.g.…”