Lifetime Number of Mates Interacts with Female Age to Determine Reproductive Success in Female Guppies

Jonathan P Evans,Sean Walker

doi:10.1371/journal.pone.0047507

Abstract

In many species, mating with multiple males confers benefits to females, but these benefits may be offset by the direct and indirect costs associated with elevated mating frequency. Although mating frequency (number of mating events) is often positively associated with the degree of multiple mating (actual number of males mated), most studies have experimentally separated these effects when exploring their implications for female fitness. In this paper I describe an alternative approach using the guppy Poecilia reticulata, a livebearing freshwater fish in which females benefit directly and indirectly from mating with multiple males via consensual matings but incur direct and indirect costs of mating as a consequence of male sexual harassment. In the present study, females were experimentally assigned different numbers of mates throughout their lives in order to explore how elevated mating frequency and multiple mating combine to influence lifetime reproductive success (LRS) and survival (i.e. direct components of female fitness). Under this mating design, survival and LRS were not significantly affected by mating treatment, but there was a significant interaction between brood size and reproductive cycle (a correlate of female age) because females assigned to the high mating treatment produced significantly fewer offspring later in life compared to their low-mating counterparts. This negative effect of mating treatment later in life may be important in these relatively long-lived fishes, and this effect may be further exacerbated by the known cross-generational fitness costs of sexual harassment in guppies.

Highlights

Female multiple mating, where females mate with two or more males within a single reproductive episode, is taxonomically widespread among sexually reproducing animals [1]
While much of this work reveals that females can obtain either direct or indirect benefits by mating with multiple males [6,7], there is accumulating evidence that conflicts of interest between the sexes over optimal mating rates can result in fitness costs, rather than benefits, for multiply-mated females [8,9]
Summed over a female’s lifespan, there was no significant difference in the total number of offspring produced by females assigned to the LM and HM treatments

Summary

Introduction

Female multiple mating, where females mate with two or more males within a single reproductive episode, is taxonomically widespread among sexually reproducing animals [1]. Studies of female multiple mating that generate estimates of lifetime reproductive success (LRS) are useful because they consider potential costs associated with elevated mating rates that may be specific to particular phases of a female’s lifespan. Females with relatively high mating rates can suffer reductions in longevity [12] and earlier onset of reproductive senescence [13] Such costs may be missed in cross-sectional studies that focus on components of female reproductive success at a specific point in time. Among studies that have generated estimates of LRS when assessing the benefits of female multiple mating, there is evidence that the direct benefits can be sufficient to outweigh any direct costs of mating [14,15,16]. Such studies are relatively scarce, and not all of the available evidence from LRS studies supports the hypothesis that multiple mating is selectively advantageous for females [17]

Methods

Results

Conclusion