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

Abstract

How males and females contribute to joint reproductive success has been a long-standing question in sexual selection. Under postcopulatory sexual selection, paternity success is predicted to derive from complex interactions among females engaging in cryptic female choice and males engaging in sperm competition. Such interactions have been identified as potential sources of genetic variation in sexually selected traits but are also expected to inhibit trait diversification. To date, studies of interactions between females and competing males have focused almost exclusively on genotypes and not phenotypic variation in sexually selected traits. Here, we characterize within-and between-sex interactions in Drosophila melanogaster using isogenic lines with heritable variation in both male and female traits known to influence competitive fertilization. We confirmed, and expanded on, previously reported genotypic interactions within and between the sexes, and showed that several reproductive events, including sperm transfer, female sperm ejection, and sperm storage, were explained by two-and three-way interactions among sex-specific phenotypes. We also documented complex interactions between the lengths of competing males' sperm and the female seminal receptacle, which are known to have experienced rapid female-male co-diversification. Our results highlight the nonindependence of sperm competition and cryptic female choice and demonstrate that complex interactions between the sexes do not limit the ability of multivariate systems to respond to directional sexual selection.

Drosophila oocyte proteome composition covaries with female mating status

“…We also predict that variation in oocyte investment will be dependent on interactions with male genotype or phenotype. Female × male interactions have been shown to extensively influence postmating reproductive events in D. melanogaster 52 , including egg volume 53 . In addition, male quality may also influence oocyte investment.…”

Age‐specific sensitivity of sperm length and testes size to developmental temperature in the bruchid beetle

“…Following artificial selection for long and short sperm in males and long and short seminal receptacle (SR) length in females, Miller & Pitnick (2002) showed that long‐sperm males outcompeted short‐sperm males when the competition took place in females with long SRs. There was no difference in sperm competitive advantage (P 2 ) between the long and short sperm when sperm competition took place within short SRs (also see Lüpold et al, 2016, Lüpold, 2020b for confirmation). Furthermore, in the zebra finch ( Taeniopygia guttata ), Bennison et al, (2015) found males with longer sperm to outcompete males with shorter sperm, whilst in the dung beetle ( Onthophagus taurus ), García‐González & Simmons (2007) found fertilization success was biased towards males with shorter sperm.…”

“…(2006). The functional significance of sperm length has been explored in relation to the evolution of sperm flagellum and mid‐piece length in vertebrates, linking it to faster swimming abilities in response to sperm competition (Fitzpatrick et al ., 2009; Lüpold et al ., 2009; Gómez Montoto et al ., 2011; also see Lüpold et al ., 2020a). Furthermore, some comparative studies reporting an association between sperm competition risk and sperm length (LaMunyon & Ward, 1999; Morrow & Gage, 2000; Byrne et al ., 2003), although other studies found no association (Hosken, 1997; Rugman‐Jones & Eady, 2007).…”

Structural dissimilarity of partners' immune genes increases sperm viability in women's reproductive tract

“…Along with precopulatory mate choice, it has been demonstrated that in many species mate choice continues after copulation, at the gamete level (Evans et al., 2012; Gasparini & Pilastro, 2011; Geßner et al., 2017; Lenz et al., 2018; Rosengrave et al., 2016; Wedekind et al., 1996; Yeates et al., 2009) and that the interactions between sperm and the female reproductive tract (FRT) play an important role in the process (Firman et al., 2017; Fitzpatrick et al., 2020; Kekäläinen & Evans, 2018; Lüpold et al., 2020). Thus, whereas the FRT has been long thought as a passive arena where a sperm race for egg fertilization is taking place, we now know that sperm–FRT interactions play a key function in shaping the reproductive success of both sexes (Holt & Fazeli, 2015).…”