American Society of Naturalists

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“Shifts in reproductive investment in response to competitors lowers male reproductive success”

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Foteini Spagopoulou, Regina Vega-Trejo, Megan L. Head, and Michael D. Jennions (Sep 2020)

The presence of sexual competition lowers male reproductive success in the G. holbrooki mosquitofish

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Increased male-male competition for access to females decreases sperm speed, reduces copulation attempts and courtship displays, and most importantly, lowers male reproductive success

<i>Gambusia holbrooki</i> mating attempt, with male (bottom) performing a gonopodial thrust, by swinging his gonopodium (an intromittent organ modified from the anal fin) forward and trying to insert it into the gonopore of the female (top).<br />(Credit: Ellen Gearing)
Gambusia holbrooki mating attempt, with male (bottom) performing a gonopodial thrust, by swinging his gonopodium (an intromittent organ modified from the anal fin) forward and trying to insert it into the gonopore of the female (top).
(Credit: Ellen Gearing)

Males of many species are exposed to highly variable social environments, where the presence and intensity of competition for access to females often change. In response, males can strategically adjust their investment in behavioral or morphological traits associated with higher mating or fertilization success. For instance, males can perceive an overabundance of other males as a signal for increased sexual competition and scale up investment in sexually selected traits. However, does such an increase in investment always lead to higher reproductive success?

In a new study, Foteini Spagopoulou, Regina Vega-Trejo, Megan Head, and Michael Jennions from Uppsala University and the Australian National University, use the eastern mosquitofish (Gambusia holbrooki) to investigate whether a competitive environment drives males to increase their investment in sexually selected traits and ultimately maximize their reproductive success. Males are housed for a full spermatogenesis cycle in either a competitive treatment, by continually being exposed to cues that rivals are present, which mimics mating competition, or in a control treatment where such cues are absent. The authors first collect sperm measurements and then allow the males, following sperm replenishment, to compete freely with a similar-sized male (from the alternative treatment) for female access and copulations. Moreover, in contrast to previous studies, the authors specifically ask how male investment in sperm and mating traits ultimately translates in reproductive success using paternity testing.

Contrary to theoretical expectations, the authors observe that males from the competitive treatment have slower swimming sperm, make fewer copulation attempts and courtship displays, and most importantly, sire fewer offspring. The unanticipated outcome of exposure to cues from rivals is, therefore, making males less, rather than more, reproductively successful. The authors discuss several possible explanations and highlight the importance of exposure duration to rivals. Moreover, these findings shed a critical perspective on experimental design and stress the need of testing whether observed changes in sexual traits elevate reproductive success.


Abstract

In many species, males exhibit phenotypic plasticity in sexually selected traits when exposed to social cues about the intensity of sexual competition. To date, however, few studies have tested how this plasticity affects male reproductive success. We initially tested whether male mosquitofish, Gambusia holbrooki (Poeciliidae), change their investment in traits under pre- and post- copulatory sexual selection depending on the social environment. Focal males were exposed, for a full spermatogenesis cycle, to visual and chemical cues of rivals that were either present (competitive treatment) or absent (control). Males from the competitive treatment had significantly slower swimming sperm, but did not differ in sperm count from control males. When two males competed for a female, competitive treatment males also made significantly fewer copulation attempts and courtship displays than control males. Further, paternity analysis of 708 offspring from 148 potential sires, testing whether these changes in reproductive traits affected male reproductive success, showed that males previously exposed to cues about the presence of rivals sired significantly fewer offspring when competing with a control male. We discuss several possible explanations for these unusual findings.