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.

Keywords: Coercive mating; Poeciliidae; ejaculation; mating effort; reproductive costs.

Figure 1

Effect of investment in pre‐ and postcopulatory components of reproduction by male G. holbrooki on somatic growth. Pre‐treatment body dimensions of all experimental males are represented by the black regression line. Post‐treatment body dimensions of males experiencing the three treatments: naïve (red); mating only (green); mating andejaculation (blue) are shown along with regression lines and respective 95% confidence intervals.

Figure 2

Violin plots showing the effect of investment in pre‐ and postcopulatory components of reproduction by male G. holbrooki on (A) immune response, (B) male attractiveness, (C) male mate choice (preference for the larger of two females), and (D) number of mating attempts. Colors represent the three treatments: naïve (red); mating only (green); mating and ejaculation (blue). One male outlier (dark green point in [D]) was excluded from the statistical analyses. Letters represent significant differences among treatments based on Tukey's tests. Black bars represent mean ± SE

Figure 3

The effects of cumulative investment into mating effort (either with or without ejaculation) on the sperm traits of G. holbrooki, controlling for male body size. Effect of the three mating treatments (no investment in mating by naïve males [red], investment in mating only [green], or mating and ejaculation [blue]) on (A) total sperm count, (B) rate of sperm replenishment, and (C) sperm velocity. The sample distribution, regression line, and its 95% confidence interval for the three treatments are shown. Points with darker colors represent outliers excluded from the statistical analyses.