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

Abstract

Sex differences in morphology, physiology, development, and behavior are widespread, yet the sexes inherit nearly identical genomes, causing most traits to exhibit strong and positive cross‐sex genetic correlations. In contrast to most other traits, estimates of cross‐sex genetic correlations for fitness and fitness components ( ) are generally low and occasionally negative, implying that a substantial fraction of standing genetic variation for fitness might be sexually antagonistic (i.e., alleles benefitting one sex harm the other). Nevertheless, while low values of are often regarded as consequences of sexually antagonistic selection, it remains unclear exactly how selection and variation in quantitative traits interact to determine the sign and magnitude of , making it difficult to relate empirical estimates of cross‐sex genetic correlations to the evolutionary processes that might shape them. We present simple univariate and multivariate quantitative genetic models that explicitly link patterns of sex‐specific selection and trait genetic variation to the cross‐sex genetic correlation for fitness. We show that provides an unreliable signal of sexually antagonistic selection for two reasons. First, is constrained to be less than the cross‐sex genetic correlation for traits affecting fitness, regardless of the nature of selection on the traits. Second, sexually antagonistic selection is an insufficient condition for generating negative cross‐sex genetic correlations for fitness. Instead, negative fitness correlations between the sexes ( can only emerge when selection is sexually antagonistic and the strength of directional selection on each sex is strong relative to the amount of shared additive genetic variation in female and male traits. These results imply that empirical tests of sexual antagonism that are based on estimates of will be conservative and underestimate its true scope. In light of these theoretical results, we revisit current data on and sex‐specific selection and find that they are consistent with the theory.

Genetic covariances promote climatic adaptation in AustralianDrosophila*

“…The different results of these studies, relative to ours, could reflect differences in the traits under consideration, or the specific environmental contexts in which sex-specific selection was evaluated. For example, sexual antagonism appears to be particularly common among sexually selected traits and phenotypes mediating adult fitness components, compared to traits affecting viability (Chippindale et al 2001;Lewis et al 2011;Gosden et al 2012;Connallon and Matthews 2019). Theory also predicts that sexually antagonistic selection is more likely to emerge in relatively stable or benign environments compared to stressful ones (reviewed in Connallon and Hall 2018), which has garnered some empirical support (Long et al 2012;Berger et al 2014;De Lisle et al 2018; but see Holman L and Jacomb 2017;Martinossi-Allibert et al 2018).…”

Sex-Specific Genetic Architecture Of Behavioral Traits In A Spider

“…credible intervals in all assessed behaviors. Taken together, and also considering that empirical tests of sexual conflict that are based on the cross-sex genetic correlation for fitness are conservative (Connallon and Matthews 2019), our results imply that individual variation in aggression and activity might stem from sex-specific selection acting on these traits, and that the genetic architecture of these behaviors is sex-specific, allowing their sex-independent evolution.…”

Sexual dimorphism explains residual variance around the survival‐reproduction tradeoff in lizards: Implications for sexual conflict over life‐history evolution*

“…For example, strong sexual selection is predicted to efficiently remove deleterious mutations, many of which would also influence survival (Agrawal ; Siller ; Radwan ; Whitlock & Agrawal ; Connallon et al. ). Therefore, strong sexual selection for large male size, as represented by male‐larger SSD, may indirectly improve survival by reducing mutation load, thereby, indirectly allowing females to optimize the tradeoff between survival and reproduction.…”

“…This could indicate the general absence of sexual conflict over survival and reproductive investment in these species, or it could reflect a beneficial effect of strong sexual selection on males. For example, strong sexual selection is predicted to efficiently remove deleterious mutations, many of which would also influence survival (Agrawal 2001;Siller 2001;Radwan 2004;Whitlock & Agrawal 2009;Connallon et al 2019). Therefore, strong sexual selection for large male size, as represented by male-larger SSD, may indirectly improve survival by reducing mutation load, thereby, indirectly allowing females to optimize the tradeoff between survival and reproduction.…”