Climatic factors and species range position predict sexually antagonistic selection across taxa

Abstract

Sex differences in selection are ubiquitous in sexually reproducing organisms. When the genetic basis of traits is shared between the sexes, such sexually antagonistic selection (SAS) creates a potential constraint on adaptive evolution. Theory and laboratory experiments suggest that environmental variation and the degree of local adaptation may all affect the frequency and intensity of SAS. Here, we capitalize on a large database of over 700 spatially or temporally replicated estimates of sex-specific phenotypic selection from wild populations, combined with data on microclimates and geographical range information. We performed a meta-analysis to test three predictions from SAS theory, that selection becomes more concordant between males and females: (1) in more stressful environments, (2) in more variable environments and (3) closer to the edge of the species' range. We find partial empirical support for all three predictions. Within-study analyses indicate SAS decreases in extreme environments, as indicated by a relationship with maximum temperature, minimum precipitation and evaporative potential (PET). Across studies, we found that the average level of SAS at high latitudes was lower, where environmental conditions are typically less stable. Finally, we found evidence for reduced SAS in populations that are far from the centre of their geographical range. However, and notably, we also found some evidence of reduced average strength of selection in these populations, which is in contrast to predictions from classical theoretical models on range limit evolution. Our results suggest that environmental lability and species range position predictably influence sex-specific selection and sexual antagonism in the wild.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

Understanding the evolution of ecological sex differences: Integrating character displacement and the Darwin-Bateman paradigm

“…; De Lisle et al. ). Moreover, a number of recent studies have highlighted the potential contribution of sexual dimorphism and SA selection to community dynamics (Fryxell et al.…”

The ecology of sexual conflict: Temperature variation in the social environment can drastically modulate male harm to females

“…Sexual conflict unfolds via two fundamentally distinct processes: intra‐locus sexual conflict (IASC), when the trait/s under sexually antagonistic selection share the same underlying loci (e.g., different optima for the same trait in males and females), or inter‐locus sexual conflict (IRSC), when sexually antagonistic selection targets different loci in both sexes (e.g., male adaptations involving one trait and female counter‐adaptations involving a different trait). Recent work has emphasized that both IASC and IRSC must be understood in its ecological setting (Gomez‐Llano, Bensch, & Svensson, ; De Lisle, Goedert, Reedy, & Svensson, ; Martinossi‐Allibert, Arnqvist, & Berger, ; Perry, Garroway, & Rowe, ; Perry & Rowe, ). On the one hand, several studies over the last few years have shown that IASC can be strongly modulated by the environment so that inter‐sexual correlations in fitness can change significantly across environments (Berger et al, ; Long, Agrawal, & Rowe, ; Punzalan, Delcourt, & Rundle, , but see Delcourt, Blows, & Rundle, ; Martinossi‐Allibert, Savkovic et al, ; Punzalan et al, ).…”

Cross-sex genetic correlations for fitness and fitness components: Connecting theoretical predictions to empirical patterns

“…Second, an even larger number of studies have published empirical estimates of female‐ and male‐specific selection on homologous traits that both sexes express (Cox and Calsbeek ; Morrissey ; De Lisle et al. ; Singh and Punzalan ). These data provide clear evidence of sexually antagonistic selection in cases where female and male selection gradients of a trait exhibit opposite signs ( β f β m < 0; e.g., Cox and Calsbeek ; Morrissey ; Sanjaka et al.…”

“…Equation can also be expressed as a function of sex‐specific linear selection gradients, β f and β m , which are widely estimated in animal populations (Cox and Calsbeek ; Morrissey ; De Lisle et al. ; Singh and Punzalan ). Provided the trait is genetically variable (), the criterion for becomes: where γ f and γ m represent the strengths of stabilizing selection on each sex ( and ).…”