The measure and significance of Bateman's principles

Abstract

Bateman's principles explain sex roles and sexual dimorphism through sex-specific variance in mating success, reproductive success and their relationships within sexes (Bateman gradients). Empirical tests of these principles, however, have come under intense scrutiny. Here, we experimentally show that in replicate groups of red junglefowl, Gallus gallus, mating and reproductive successes were more variable in males than in females, resulting in a steeper male Bateman gradient, consistent with Bateman's principles. However, we use novel quantitative techniques to reveal that current methods typically overestimate Bateman's principles because they (i) infer mating success indirectly from offspring parentage, and thus miss matings that fail to result in fertilization, and (ii) measure Bateman gradients through the univariate regression of reproductive over mating success, without considering the substantial influence of other components of male reproductive success, namely female fecundity and paternity share. We also find a significant female Bateman gradient but show that this likely emerges as spurious consequences of male preference for fecund females, emphasizing the need for experimental approaches to establish the causal relationship between reproductive and mating success. While providing qualitative support for Bateman's principles, our study demonstrates how current approaches can generate a misleading view of sex differences and roles.

Characterizing the reproductive transcriptomic correlates of acute dehydration in males in the desert-adapted rodent,Peromyscus eremicus

“…Indeed, given that the physiological demands of reproduction are purportedly greater in females, though this is controversial, (Bateman's Principle: proposed in [115]; addressed in [116]; reviewed in [117]; tested in [118][119][120]), we would expect to see a greater degree of reproductive suppression in females. While such work is beyond the scope of this manuscript, we hope that future research will evaluate female cactus mouse reproductive responses to dehydration.…”

With our powers combined: integrating behavioral and genetic data to estimate mating success and sexual selection

“…By combining behavioral and genetic data in a common framework, our analysis embraced multiple aspects of mating success over the course of the experiment. Combining genetic data and behavioral observations in order to account for mating acts the offspring of which were not sampled was also adopted for instance by Collet et al (2014) and Pélissié et al (2014) but their approach relied on complete knowledge of copulation events in the mating group to disentangle the contribution of precopulatory and post-copulatory components of reproductive success. Our approach consisted in merging the behavioral and genetic datasets, both incomplete -a common situation in ecology and evolution -, and taking advantage of the conditional structure of the successive components of mating success: visit, simultaneous gamete release and offspring production.…”

“…Similarly, a non-zero value can also carry more information than just the total reproductive success between a pair of individuals, since it can be the outcome of a variable number of matings, which is of importance to measure reproductive investment. In this perspective, matrices of copulation success as obtained by direct observations of mating behavior obviously contain data that are complementary to parentage assignation methods (Collet et al 2014). We therefore need statistical models integrating both behavioral and genetic data to provide estimates of the various definitions of mating success, by disentangling pre-copulatory and post-copulatory components as already suggested by several authors (Arnold and Wade 1984a, Pischedda and Rice 2012, Pélissié et al 2014.…”

“…It is noteworthy that the definition of mating success is to a great extent constrained by methodological possibilities. Standard methodological approaches using parental tables obtained from genetic assignations can only target the number of individuals with which progeny of the focal individual is produced and generally result in biased estimates (Collet et al 2014). These approaches deduce individual mating success by counting the number of non-zero elements on the individual line of the parental table.…”

“…An estimate of such matrix is typically generated by parentage analysis based on genetic markers (e.g. Garant et al 2001, Jones and Ardren 2003, Jones et al 2004) possibly complemented by direct observations of mating behavior (Pemberton et al 1992, Coltman et al 1999, Collet et al 2014.…”