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

Abstract

Many studies ask whether young or older males are better at acquiring mates. Even so, how age affects reproductive success is still poorly understood because male age and mating history are confounded in most studies: older males usually have more mating experience. To what extent does mating history rather than age explain variation in male mating success? And how do mating history and male age determine paternity when there is also postcopulatory sexual selection? Here, we experimentally manipulated the mating history of old and young males in the eastern mosquitofish (Gambusia holbrooki). We then recorded male mating behavior and share of paternity (1259 offspring from 232 potential sires) when they competed for mates and fertilizations.Old males, and males with no mating experience, spent significantly more time approaching females, and attempting to mate, than did young males and those with greater mating experience. Male age and mating history interacted to affect paternity: old males benefited from having previous mating experience, but young males did not. Our results highlight that the age-related changes in male reproductive traits and in paternity that have been described in many taxa may be partly attributable to male mating history and not simply to age itself.

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

“…This explanation is further supported by our recent experimental studies of the same mosquitofish population where older males achieved significantly higher paternity success than young males (Aich et al. 2021a, b). These results are intriguing, because they support our hypothesis that old male mosquitofish do not show any decline in reproduction success or offspring quality once past mating effort is experimentally controlled.…”

“…Third, irrespective of paternal mating history, the sons of older males, to some extent, made more copulation attempts than sons of younger males (p = 0.033). This implies there is evidence of epigenetic heritability of this behavioral trait as we have elsewhere shown that older fathers make more mating attempts (Aich et al 2021a). Overall, our results provide evidence that paternal effects might alter the strength of sexual selection on precopulatory and postcopulatory reproductive traits, establishing an intergenerational link between ageing and sexual selection (Monaghan et al 2020;Vuarin et al 2021).…”

“…Mosquitofish females have an average postmaturation lifespan of 12–15 months, but far less for males (see Aich et al. 2021a for details). Autumn‐born females in this species often breed alongside their spring‐born offspring the following year, but this seasonal overlap is absent for males (Pyke 2005; Kahn et al.…”

“…We then used a new set of 400 breeding adult males and females 12 weeks later to rear a second set of offspring to produce "young" males. Mosquitofish females have an average postmaturation lifespan of 12-15 months, but far less for males (see Aich et al 2021a for details). Autumn-born females in this species often breed alongside their spring-born offspring the following year, but this seasonal overlap is absent for males (Pyke 2005;Kahn et al 2013).…”

Experience with mating receptivity cues affects sexual behaviour of male guppies, but not their strength of preference towards receptive females

“…Contrary to our prediction, males with social learning experience of female receptivity cues did not became choosier or increase their preference towards receptive females in dichotomous choice tests. It may be that that our experimental treatment might have changed the perception of naïve and experienced males in future reproductive opportunities, potentially biasing the investment of naïve males in sexual behaviors that we observed in the first sexual encounter of their pre-treatment test (Fischer et al, 2008, Aich et al, 2021). Furthermore, determining the costs of sexual behaviours are challenging in benign lab environments where food is not a limiting factor.…”