Darwinian sex roles confirmed across the animal kingdom

Abstract

Since Darwin's conception of sexual selection theory, scientists have struggled to identify the evolutionary forces underlying the pervasive differences between male and female behavior, morphology, and physiology. The Darwin-Bateman paradigm predicts that anisogamy imposes stronger sexual selection on males, which, in turn, drives the evolution of conventional sex roles in terms of female-biased parental care and male-biased sexual dimorphism. Although this paradigm forms the cornerstone of modern sexual selection theory, it still remains untested across the animal tree of life. This lack of evidence has promoted the rise of alternative hypotheses arguing that sex differences are entirely driven by environmental factors or chance. We demonstrate that, across the animal kingdom, sexual selection, as captured by standard Bateman metrics, is indeed stronger in males than in females and that it is evolutionarily tied to sex biases in parental care and sexual dimorphism. Our findings provide the first comprehensive evidence that Darwin's concept of conventional sex roles is accurate and refute recent criticism of sexual selection theory.

Keywords: Anisogamy; Bateman’s principles; Mating success; Sexual dimorphism; Sexual selection; parental care.

Fig. 1. Sex-biased sexual selection across the animal kingdom.

(A to C) Forest plots showing estimates of the sex bias in (A) the opportunity for selection (ΔI), (B) the opportunity for sexual selection (ΔI_s), and (C) the Bateman gradient (Δβ_ss). Effect sizes (lnCVR and Hedges’ d; see Materials and Methods) are shown with their 95% confidence intervals (CIs). Positive values indicate male-biased sexual selection parameters. Studies are grouped according to taxonomic ranks (color shades and icons).

Fig. 2. Sex-biased sexual selection and its evolutionary link to parental care and sexual dimorphism.

(A to C) Frequency distributions and global mean effect sizes (filled squares) for sex differences in (A) the opportunity for selection (ΔI), (B) the opportunity for sexual selection (ΔI_s), and (C) the Bateman gradient (Δβ_ss). (D to I) Illustration of how sex differences in Bateman’s parameters covary with (D to F) parental care and (G to I) sexual dimorphism, respectively. Error bars are 95% CIs. Different lowercase letters indicate significant differences after stepwise Bonferroni correction at α = 0.05.

Fig. 3. The sex-role syndrome.

Schematic illustration of conventional sex roles summarizing the three main findings of this study: (1) Sexual selection is stronger in males than in females, which must, by definition, be rooted in anisogamy. Stronger sexual selection on males translates in (2) female-biased parental care and (3) male-biased elaboration of traits. Arrowheads indicate direction of causality on the basis of current theory.