Nongenetic paternal effects via seminal fluid

Abstract

Mounting evidence suggests that nongenetic paternal effects on offspring may be widespread among animal taxa, but the mechanisms underlying this form of nongenetic inheritance are not yet fully understood. Here, we show that seminal fluids underlie paternal effects on early offspring survival in an insect, the cricket Teleogryllus oceanicus, and quantify the contribution of this paternal effect to the inheritance of this important fitness trait. We used castrated males within a full‐sib half‐sib experimental design to show that seminal fluid donors were responsible for variation in the survival of developing embryos to hatching, and in their subsequent survival to adulthood. Increased expression of two seminal fluid protein genes, previously found to be positively associated with sperm quality, was found to be negatively associated with embryo survival. These nongenetic paternal effects hold important implications for the evolution of adaptive maternal responses to sperm competition, and more broadly for the interpretation of sire effects from classic quantitative genetic breeding designs.

Can paternal effects via seminal fluid contribute to the evolution of polyandry?

“…In that study, the seminal fluid of some donors was found to enhance embryo viability while the seminal fluid of others reduced embryo viability. Importantly, increasing expression of ToSfp011 in the accessory glands of seminal fluid donors was associated with reduced embryo survival [19]. Taken together with the findings of our interference RNA, the data suggest that while ToSfp011 is essential for embryo development it may be harmful when abundant.…”

“…Using interference RNA, we found that at least one seminal fluid protein, ToSfp011, was essential for the development of embryos to hatching. In a previous study, we documented significant variation in embryo viability among genetically monogamous females mated to castrated seminal fluid donors [19]. In that study, the seminal fluid of some donors was found to enhance embryo viability while the seminal fluid of others reduced embryo viability.…”

“…They found that a male that imparted high viability to his own embryos did so for the embryos sired by his sperm competition rival. The precise mechanism by which ToSfp011 affects embryo viability remains uncertain; candidate mechanisms include a direct effect on embryo development if it were able to enter the egg, perhaps bound to sperm [19], or indirect through its effects on the genetic integrity of sperm themselves.…”

“…Indeed, paternal effects on embryo viability have been reported to harbour significant additive genetic variance in this species [29]. However, these paternal effects are genetically correlated with a male's expenditure on his seminal fluid producing accessory glands [29], and recent work suggests that nongenetic paternal effects of seminal fluid can largely account for the apparent genetic effects on embryo viability [19]. Alternatively it may be that castrated males were unable to deliver the full complement of seminal fluid proteins (sfps) contained within a normal ejaculate, so that females mated to castrated males did not accrue the full benefits of seminal fluid doses from multiple males.…”

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

“…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 partners against sexually transmitted diseases (Gioti et al., 2012; McGraw, Clark, & Wolfner, 2008; Peng, Grassl, Millar, & Baer, 2016, review: Avila, Sirot, LaFlamme, Rubinstein, & Wolfner, 2011; Chapman, 2001; Morrow & Innocenti, 2012; Poiani, 2006; Sirot, Wong, Chapman, & Wolfner, 2015). In addition to their immediate effects, SFPs may also be responsible for seminal fluid‐mediated transgenerational effects (Bromfield et al., 2014; Crean, Kopps, & Bonduriansky, 2014; Priest, Roach, & Galloway, 2008; Simmons & Lovegrove, 2019). Moreover, although some effects of SFPs are essential and beneficial for both parents, other functions appear sexually antagonistic (Chapman, Liddle, Kalb, Wolfner, & Partridge, 1995; Patlar, Weber, Temizyürek, & Ramm, 2020, review: Sirot et al., 2015).…”