Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies

Abstract

Polyandry, where females mate with multiple males, means that a male's reproductive success will depend both on his ability to acquire mates and the ability of his sperm to compete effectively for fertilizations. But, how do males partition their reproductive investment between these two episodes of selection? Theory predicts that increases in ejaculate investment will come at a cost to investment in other reproductive traits. Although evidence revealing such trade-offs is accumulating, we know little about their genetic basis. Here, I report patterns of genetic (co)variation for a range of traits subject to pre-and postcopulatory sexual selection in the guppy Poecilia reticulata, a promiscuous livebearing fish in which males alternate between courtship and sneak matings to obtain copulations. The analyses of genetic variation and covariation for these behaviours revealed a strong genetic predisposition for one tactic over the other. Both mating tactics were also strongly genetically integrated with the level of sexual ornamentation and ejaculate quality. Males that predominantly performed sneak matings were less ornamented but had faster swimming sperm than those that predominantly used courtship. These patterns of genetic variation and covariation reveal potential evolutionary constraints on the direction of selection of pre-and postcopulatory traits, and support sperm competition theory by revealing a trade-off between sexual attractiveness and investment in ejaculates.

Patterns of genetic variation and covariation in ejaculate traits reveal potential evolutionary constraints in guppies

“…The study complements recent quantitative genetic analyses of pre and postcopulatory sexually-selected traits in this species in which two measures of in vitro sperm performancesperm swimming velocity (average path velocity; VAP), and the proportion of live sperm per ejaculate (sperm viability)-were shown to be negatively genetically associated with male sexual behaviour and body ornamentation (Evans, 2010). The present study extends these analyses by exploring patterns of genetic covariation among ejaculate traits, adding to just handful of studies that have addressed this topic in other species (reviewed by Simmons and Moore, 2009).…”

Evolutionary Modeling Predicts a Decrease in Postcopulatory Sperm Viability as a Response to Increasing Levels of Sperm Competition

“…Here we assume that there is no direct trade-off between sperm number and viability, but a trade-off between investment in winning fertilizations (i.e., ejaculate investment) and investment in obtaining matings (for empirical evidence see Warner et al 1995;Danielsson 2001;Evans 2010;Simmons et al 2010;Engqvist 2011). As in many previous sperm competition models (e.g., Ball and Parker 1996; Parker et al 1996Parker et al , 1997Tazzyman et al 2009), this trade-off is expressed as .…”

“…Alternatively, at least in some insects, sperm viability has been shown to be accomplished by seminal fluids (Holman 2009a), which may be costly to produce. Trade-offs may also be present between investment in sperm quality and other aspects of male reproductive success, such as investment in traits affecting attractiveness and mating success (Evans 2010;Simmons et al 2010;Engqvist 2011;Preston et al 2011). Yet not much is known concerning which factors may benefit sperm viability.…”

Sexual Conflict and Sperm Competition

“…Alternatively, both sperm number and sperm quality may increase in response to sperm competition (Locatello et al 2007) potentially forcing a trade-off with nonejaculate traits. For example, ejaculate quality may trade off with attractiveness (Evans 2010;Rowe et al 2010) or immune function (Simmons 2012), and testes size has been shown to trade off with traits such as flight capability (Saglam et al 2008) and weaponry (Simmons and Emlen 2006). It is therefore possible that increased investment in ejaculates could trade off with traits that directly enhance female fitness, such as nuptial gift size or provision of parental care (e.g., Simmons et al 1993).…”