Abstract
Quantitative genetic theory proposes that phenotypic evolution is shaped by G, the matrix of genetic variances and covariances among traits. In species with separate sexes, the evolution of sexual dimorphism is also shaped by B, the matrix of between‐sex genetic variances and covariances. Despite considerable focus on estimating these matrices, their underlying biological mechanisms are largely speculative. We experimentally tested the hypothesis that G and B are structured by hormonal pleiotropy, which occurs when one hormone influences multiple phenotypes. Using juvenile brown anole lizards (Anolis sagrei) bred in a paternal half‐sibling design, we elevated the steroid hormone testosterone with slow‐release implants while administering empty implants to siblings as a control. We quantified the effects of this manipulation on the genetic architecture of a suite of sexually dimorphic traits, including body size (males are larger than females) and the area, hue, saturation, and brightness of the dewlap (a colorful ornament that is larger in males than in females). Testosterone masculinized females by increasing body size and dewlap area, hue, and saturation, while reducing dewlap brightness. Control females and males differed significantly in G, but treatment of females with testosterone rendered G statistically indistinguishable from males. Whereas B was characterized by low between‐sex genetic correlations when estimated between control females and males, these same correlations increased significantly when estimated between testosterone females and either control or testosterone males. The full G matrix (including B) for testosterone females and either control or testosterone males was significantly less permissive of sexually dimorphic evolution than was G estimated between control females and males, suggesting that natural sex differences in testosterone help decouple genetic variance between the sexes. Our results confirm that hormonal pleiotropy structures genetic covariance, implying that hormones play an important yet overlooked role in mediating evolutionary responses to selection.
Highlights
Quantitative genetics was originally developed by plant and animal breeders as a way to predict how crops and livestock would respond to artificial selection, subsequently adopted by evolutionary biologists interested in natural selection
Recent work has emphasized the importance of B in shaping the evolution of sexual dimorphism (Gosden et al 2012; Wyman et al 2013; Cheng and Houle 2020) and studies on a variety of species have empirically characterized B (Steven et al 2007; Campbell et al 2011; Lewis et al 2011; Ingleby et al 2014; Cox et al 2017a; White et al 2019), we know relatively little about the physiological mechanisms that orchestrate the breakdown of between-sex genetic covariance to facilitate the evolution of sexual dimorphism (Cox et al 2017b)
To test whether hormonal pleiotropy structures G and B, we focus on the steroid hormone testosterone, which naturally circulates at higher levels in adult males than in females
Summary
Quantitative genetic theory proposes that phenotypic evolution is shaped by G, the matrix of genetic variances and covariances among traits. In species with separate sexes, the evolution of sexual dimorphism is shaped by B, the matrix of between-sex genetic variances and covariances. We quantified the effects of this manipulation on the genetic architecture of a suite of sexually dimorphic traits, including body size (males are larger than females) and the area, hue, saturation, and brightness of the dewlap (a colorful ornament that is larger in males than in females). The full G matrix (including B) for testosterone females and either control or testosterone males was significantly less permissive of sexually dimorphic evolution than was G estimated between control females and males, suggesting that natural sex differences in testosterone help decouple genetic variance between the sexes. KEYWORDS : Animal model, Anolis, B matrix, G matrix, genetic correlation, intralocus sexual conflict, quantitative genetics, sexual dimorphism, testosterone
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