Genotype-by-environment interactions for seminal fluid expression and sperm competitive ability

Abstract

Sperm competition commonly occurs whenever females mate multiply, leading to variation in male paternity success. This can be due to variation in the various traits that might affect sperm competitive ability, which itself depends on both genetic and environmental factors, as well as on genotype‐by‐environment interactions (GEI). Seminal fluid is a major component of the male ejaculate that is often expected to mediate sperm competition, where different genotypes can differ in their seminal fluid expression as a response to different levels of sperm competition (i.e. exhibit GEI). We therefore here focussed on testing for GEI in expression of two recently identified seminal fluid transcripts, suckless‐1 and suckless‐2, which potentially modulate sperm competitive ability in the simultaneously hermaphroditic flatworm Macrostomum lignano via their effects on manipulating post‐mating partner behaviour and ultimately the fate of transferred ejaculates. In addition, we sought to test for GEI in sperm competitive ability in a standardized sperm competition (P1 and P2) assay, to investigate the relationship between natural variation in the expression of these seminal fluid transcripts generated through GEI and relative paternity success. We found GEI for the expression level of suckless‐1 and suckless‐2, as well as for sperm competitive ability. Moreover, we found a positive relation between the expression of suckless‐1 and relative paternity success (P1). This suggests that natural variation in the expression of this seminal fluid transcript indeed can influence sperm competition outcomes in M. lignano.

Seminal Fluid-Mediated Manipulation of Post-mating Behavior in a Simultaneous Hermaphrodite

“…Although perhaps not dramatic in the sense that sucking never approached 100%, we nevertheless should consider that this effect, coupled with the variation we have described, certainly implies that the effects could be significant in nature. Importantly, a separate study investigating natural variation in the expression of suckless-1 and suckless-2 generated through genotype 3 environment interactions has now revealed a strong positive correlation between suckless-1 expression and defensive sperm competitive ability, P 1 [52], supporting the notion that this protein has functionally significant effects under sperm competition.…”

Divergence of seminal fluid gene expression and function among natural snail populations

“…Many subsequent studies extensively documented within‐population variation of SFPs using inbred families from a single population, particularly focusing on the influence on sperm competition (e.g. sequence: Clark, Aguadé, Prout, Harshman, & Langley, 1995; Fiumera, Dumont, & Clark, 2005; Fiumera, Dumont, & Clark, 2007; Zhang, Clark, & Fiumera, 2013, gene expression: Patlar, Weber, & Ramm, 2019; Patlar & Ramm, 2020, protein abundance: Brandon, Heusnes, Caudle, & Fayrer‐Hosken, 1999). More direct attempts to compare SFP divergence between populations have recently begun, providing empirical support for diversified SFPs, likely associating with differential effects (protein abundance: Baer, Zareie, Paynter, Poland, & Millar, 2012; Goenaga, Yamane, Rönn, & Arnqvist, 2015; Mangels et al., 2015).…”

Seminal fluid gene expression and reproductive fitness in Drosophila melanogaster

“…normal atmosphere vs. high CO 2 concentration) than P2 in Drosophila melanogaster [48]. Moreover, variation of SFP gene expression generated through genotype-by-environment interactions in competitive and non-competitive settings found a positive relationship between gene expression and P1 but not P2 in flatworms [49]. The use of experimental evolution to enforce monogamy in Drosophila has also shown that monogamous males become weaker sperm competitors and have lower expression of SFPs, but do not differ from polygamous males in their ability to diminish female remating [50].…”