Quantifying the costs of pre- and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort

Abstract

Although it is widely stated that both mating behavior and sperm traits are energetically costly for males, we currently lack empirical estimates of the relative costs to males of pre‐ versus postcopulatory investments. Such estimates require the experimental separation of the act of mating from that of ejaculation, which is a nontrivial logistical challenge. Here, we overcome this challenge using a novel morphological manipulation (gonopodium tip ablation) in the eastern mosquitofish (Gambusia holbrooki) to tease apart investment in mating effort from that in sperm replenishment following ejaculation. We quantified the relative cumulative costs of investing in mating effort and ejaculation by comparing somatic traits and reproductive performance among three types of males: ablated males that could attempt to mate but not ejaculate; unablated males that could both mate and ejaculate; and control males that had no access to females. We show that, after eight weeks, mating investment significantly reduces both body growth and immunocompetence and results in a significant decline in mating effort. In contrast, cumulative investment into sperm replenishment following ejaculation has few detectable effects that are only apparent in smaller males. These minor costs occur despite the fact that G. holbrooki has very high levels of sperm competition and multiple mating by both sexes, which is usually associated with elevated levels of sperm production. Crucially, our study is the first, to our knowledge, to experimentally compare the relative costs of pre‐ and postcopulatory investment on components of male fitness in a vertebrate.

Does female resistance to mating select for live‐fast‐die‐young strategies in males? A comparative analysis in the genus Drosophila

“…As a result, the mean costs of pre-copulatory investment might be expected to outweigh the mean costs of post-copulatory investment for males in many species-an expectation that is consistent with the available evidence (e.g. Chung et al, 2021;Gasparini et al, 2019). Moreover, many pre-copulatory traits, such as prominent signals and weapons, can expose males to elevated risk of death from accidents and predation, which can directly reduce lifespan (albeit less so in a protected laboratory environment) as well as select for reduced investment in somatic maintenance (Kotiaho et al, 1998).…”

Disentangling the effects of male age and mating history: Contrasting effects of mating history on precopulatory mating behavior and paternity success

“…Males expend considerable time and energy attempting to mate, making up to one mating attempt per minute (Bisazza and Marin 1995;Wilson 2005). Past mating effort is therefore likely to affect a male's current mating behavior (Chung et al 2021;but see Iglesias-Carrasco et al 2019a). In addition, to improve our ability to quantify the effects of male age and mating history on male reproductive success, we statistically accounted for other known sources of variation.…”

“…Past mating effort is therefore likely to affect a male's current mating behavior (Chung et al. 2021; but see Iglesias‐Carrasco et al. 2019a).…”

Separating the effects of paternal age and mating history: Evidence for sex‐specific paternal effect in eastern mosquitofish

“…One distinction between our current study and the earlier one is that mated males in our current study were in the mating treatment for 2 weeks rather than for their entire life. These males, therefore, incurred lower costs of repeatedly mating and replenishing sperm (Chung et al 2021). It is possible that the assigned period of mating was insufficient to reveal negative effects associated with repeated mating for some traits.…”

“…These males, therefore, incurred lower costs of repeatedly mating and replenishing sperm (Chung et al. 2021). It is possible that the assigned period of mating was insufficient to reveal negative effects associated with repeated mating for some traits.…”