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 characteristics 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 26 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 26 candidates, we identified eight genes that affect P1 when knocked down in females, and showed that five of them do so when knocked down in the female nervous system. In particular, Rim knockdown in sensory pickpocket (ppk)+ neurons lowered P1, confirming previously published results, and a novel candidate, caup, lowered P1 when knocked down in octopaminergic Tdc2+ neurons. These results demonstrate that specific neurons in the female’s nervous system play a functional role in sperm competition and expand our understanding of the genetic, neuronal, and mechanistic basis of female responses to multiple matings. We propose that these neurons in females are used to sense, and integrate, signals from courtship or ejaculates, to modulate sperm competition outcome accordingly.

Genetic Factors Influencing Sperm Competition

“…Among the genetic factors that we can safely deem as sperm competition genes, we observe a remarkable breadth of biological roles, a marked pleiotropic nature in many of them, and multiple examples of genes not expressed in testes or the sperm (∼56% in Table 1 ). Importantly, staggering evidence supports that the fertilization bias that results from post-copulatory male–male competition can be exerted by genes whose effects not only manifest through the males but also through the females (Chen et al, 2019). Nevertheless, this gene list is still limited, and biased toward D. melanogaster and research foci such as the characterization of the male accessory glands of this species.…”

“…Multiply mated females can also bias competitive outcomes through their nervous system, which is known to be important for proper sperm storage (Arthur et al, 1998). For example, a neuron-specific sensory knockdown in females of the D. melanogaster gene Rab3 interacting molecule ( Rim ), a gene that mediates neurotransmitter secretion, lowers males P1 (Chow et al, 2013; Chen et al, 2019). Similarly in D. melanogaster , the gene Caupolican ( caup ), which is generally involved in neuronal development, has been shown to affect males P1 when knockdown in female’s octopaminergic neurons, and both P1 and P2 but not overall fertility when knockdown across the whole nervous system of the female (Chen et al, 2019).…”

“…For example, a neuron-specific sensory knockdown in females of the D. melanogaster gene Rab3 interacting molecule ( Rim ), a gene that mediates neurotransmitter secretion, lowers males P1 (Chow et al, 2013; Chen et al, 2019). Similarly in D. melanogaster , the gene Caupolican ( caup ), which is generally involved in neuronal development, has been shown to affect males P1 when knockdown in female’s octopaminergic neurons, and both P1 and P2 but not overall fertility when knockdown across the whole nervous system of the female (Chen et al, 2019). Overall, both octopaminergic Tdc2 + and proprioceptive ppk + neurons, which innervate the female reproductive tract, have been found to play roles in competitive settings.…”

“…Overall, both octopaminergic Tdc2 + and proprioceptive ppk + neurons, which innervate the female reproductive tract, have been found to play roles in competitive settings. Although the precise mechanisms whereby this type of neural-related genes affects sperm storage are still unknown, it has been proposed that this could happen by how the female nervous system integrates signals from courtship and ejaculates (Chen et al, 2019).…”

TheDrosophilaseminal proteome and its role in postcopulatory sexual selection

“…The availability of D. melanogaster lines with GFP-or RFP-labelled sperm also allows the unravelling of PCSS mechanisms via direct quantification of rival male sperm storage and sperm utilization within the female reproductive tract [13,50]. These methods and tools have allowed researchers to uncover roles of Sfps in PCSS and to dissect the relative roles of males and females [51,52]. The main approaches to ascertaining the role of Sfps in paternity share or sperm dynamics have been (i) association studies, which examine correlations between the traits of interest and natural variation in Sfp alleles, and (ii) functional genetic studies, involving the genetic manipulation of Sfps, or the cells and tissues that produce them.…”