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

Abstract

Seminal fluid proteins (SFPs, also referred to as accessory gland proteins or ACPs) contained in the ejaculate are transferred together with sperm to mating partners. Laboratory studies have examined within-population variation of SFPs at sequence, expression and functional levels, and established that these proteins exhibit a wide range of functions, such as inducing ovulation or defending mating

Seminal fluid protein divergence among populations exhibiting postmating prezygotic reproductive isolation

“…While our results show divergence in Sfp abundance is a potential mechanism underlying the asymmetry and occurrence of PMPZ isolation between D. montana populations, further studies are required to discern any causal relationship. A recent study showed ectopic injection of divergent Sfps between freshwater snail populations was associated with differences in the effects of these Sfps on fecundity and sperm transfer (Nakadera et al, 2020).…”

“…While our results show divergence in Sfp abundance is a potential mechanism underlying the asymmetry and occurrence of PMPZ isolation between D. montana populations, further studies are required to discern any causal relationship. A recent study showed ectopic injection of divergent Sfps between freshwater snail populations was associated with differences in the effects of these Sfps on fecundity and sperm transfer (Nakadera et al., 2020). PMPZ isolation in D. montana may also result from differences between populations in sperm length and female sperm storage organ morphology, direct interactions between the sperm and egg cell surfaces, or a combination of these factors (Howard et al., 2009).…”

“…Moreover, differences in Sfp expression between species, and abnormal gene expression profiles or changes in protein abundance in the female reproductive tract after mating with heterospecific vs. conspecific males are associated with PMPZ isolation (Ahmed‐Braimah et al., 2017; Bono et al., 2011; McCullough et al., 2020). Recently, ectopic injection of Sfps between populations of simultaneously hermaphroditic freshwater snails, Lymnaea stagnalis , that showed divergent gene expression patterns was shown to alter fecundity and sperm transfer (Nakadera et al., 2020). These shared patterns of divergence between taxa supports a putative role of Sfps as causative agents of PMPZ isolation.…”

“…However, while studies showing divergence in gene expression are associated with disrupted ejaculate × female reproductive tract interactions, changes in gene expression may not correlate with changes in protein abundance (Wang et al., 2019), where the molecular interactions causing PMPZ isolation take place. Divergence in protein identity or abundance between taxa could disrupt ejaculate × female reproductive tract interactions, leading to PMPZ isolation (Goenaga et al., 2015; Nakadera et al., 2020). High‐throughput proteomics using liquid chromatography tandem mass spectrometry (LC‐MS/MS) has revolutionized identification and quantification of Sfps, revealing that the male ejaculate often contains hundreds of unique proteins (Bayram et al., 2019; Karr, 2019; McDonough et al., 2016; Rowe et al., 2019; Whittington et al., 2019).…”

Unprecedented dynamics of seminal fluid replenishment after mating

“…192 h is sufficient for these snails to become fully motivated to copulate as male (Van Duivenboden and Ter Maat 1985), based on the completed filling state of their prostate glands (De Boer et al 1997). Moreover, previous studies showed that virgin snails show reduced SFP production (Nakadera et al 2019(Nakadera et al , 2020. Therefore, we predicted that SFP production would be very low one week after mating in this species.…”