The evolution of sex roles: The importance of ecology and social environment

Abstract

Males and females often have different roles in reproduction, although the origin of these differences has remained controversial. Explaining the enigmatic reversed sex roles where males sacrifice their mating potential and provide full parental care is a particularly long-standing challenge in evolutionary biology. While most studies focused on ecological factors as the drivers of sex roles, recent research highlights the significance of social factors such as the adult sex ratio. To disentangle these propositions, here, we investigate the additive and interactive effects of several ecological and social factors on sex role variation using shorebirds (sandpipers, plovers, and allies) as model organisms that provide the full spectrum of sex role variation including some of the best-known examples of sex-role reversal. Our results consistently show that social factors play a prominent role in driving sex roles. Importantly, we show that reversed sex roles are associated with both male-skewed adult sex ratios and high breeding densities. Furthermore, phylogenetic path analyses provide general support for sex ratios driving sex role variations rather than being a consequence of sex roles. Together, these important results open future research directions by showing that different mating opportunities of males and females play a major role in generating the evolutionary diversity of sex roles, mating system, and parental care.

Keywords: adult sex ratio; habitat productivity; mating system; parental care; sex-role reversal.

Fig. 1.

Distribution of (A) mating systems and parental care and (B) ecological and social variables in 41 shorebird species included in the study. In panel (A), the colored circles show 1) parental care score bias (outer circle) and 2) polygamy bias (inner circle). The latter variable is represented either by polygamy frequency bias (most species) or by polygamy score bias (three species without polygamy frequency data, see SI Appendix, Table S5). In panel (B), the colored circles show 1) habitat productivity (outer circle, light and dark green), 2) hatching success (second circle, light and dark brown), 3) breeding density (third circle, gray and black), and 4) adult sex ratio (inner circle, pink and blue). Light and dark colors represent an average value for the species lower or higher, respectively, than the median in habitat productivity, hatching success, and breeding density. For adult sex ratio, pink and blue colors represent an average value for the species lower or higher, respectively, than 0.5 (i.e., even sex ratio). The phylogenetic relationships are shown according to a supertree of shorebirds (77). Silhouette images represent from bottom following clockwise direction: Calidris pugnax^a, Actitis hypoleucos, L. limosa^a, Jacana spinosa, Charadrius alexandrinus, V. vanellus^b, Haematopus ostralegus, Recurvirostra americana^a (source: http://www.phylopic.org/). ^ab reproduced here under a Creative Commons Attribution 3.0 Unported license (https://creativecommons.org/licenses/by/3.0/) and were generated by ^aAlexandre Vong and ^bNina Skinner. The remaining figures are public domain.

Fig. 2.

Components of sex roles (response variables) in relation to ecology (habitat productivity, hatching success) and social environment (adult sex ratio and breeding density). Panels show regression lines estimated by multipredictor PGLS models (blue: significant; black: not significant) and their SE (gray shading). (A) Polygamy frequency bias, (B) polygamy score bias, (C) parental care score bias, and (D) parental care duration bias. See Table 1 legend and Materials and Methods in the main text for definitions of variables. See Table 1 for details of the statistical models and sample sizes.

Fig. 3.

Interactive effects (A) between adult sex ratio and breeding density and (B) between breeding density and habitat productivity on polygamy frequency bias (response variable). Adult sex ratio and breeding density are expressed as species estimates from raw data. See Table 1 legend and Materials and Methods in the main text for variables’ explanation. Lines represent predictions for different values of (A) breeding density and in (B) habitat productivity (one SD higher than average: full black line, average: long dashed dark gray line, one SD lower than average: small dashed light gray line). N = 36 species.

Fig. 4.

Best-supported phylogenetic path models of sex role components and ecological and social predictor variables. Path analyses supported either Model 1a or Model 2a (or both) against alternative scenarios depending on which variables were used to represent parental care bias and mating system bias (see SI Appendix, Table S3 for model comparisons and SI Appendix, Fig. S2 for the full model set). Red and blue arrows indicate significant positive and negative relationships, respectively; dashed gray arrows show nonsignificant relationships.