The evolution of androgen receptor expression and behavior in Anolis lizard forelimb muscles

Abstract

The motor systems that produce behavioral movements are among the primary targets for the action of steroid hormones, including androgens. Androgens such as testosterone bind to androgen receptors (AR) to induce physiological changes in the size, strength, and energetic capacity of skeletal muscles, which can directly influence the performance of behaviors in which those muscles are used. Because tissues differentially express AR, resulting in tissue-specific sensitivity to androgens, AR expression may be a major target of selection for the evolution of behavior. Anolis lizards (i.e., anoles) provide a robust system for the study of androgen-regulated traits, including the behavioral traits that facilitate social display and locomotion. In this study, we examined six anole species that demonstrate significant variation in the behavioral use of the forelimbs to measure the proportion of myonuclei in the bicep muscles that express AR. Using phylogenetic comparative analyses, we found that species with a greater proportion of nuclei positive for AR expression in the biceps exhibited greater frequencies of locomotor movements and pushup displays. These results suggest that AR expression in skeletal muscles may influence the evolution of androgen-regulated behaviors in this group.

Seasonal regulation of behaviour: what role do hormone receptors play?

“…Variation across species, sexes and individuals in levels of AR expression in peripheral tissues have been associated with differential expression of a variety of behaviours. For example, AR expression in muscles covaries with the expression of courtship display in birds [104], social and sexual behaviour in fish [105], and display and locomotor behaviours in lizards [106]. In birds, experimental manipulations have confirmed a functional link between peripheral AR activation and courtship and vocal behaviours [107,108].…”

Morphological evidence of sexual dimorphism in a Continental anole species of southeastern of Mexico

“…In the genus Anolis, differences in foreleg length between males and females have been shown to be related to the number of androgen receptors present in each sex (Johnson et al 2018). These receptors are correlated with the number of push-ups that a male can perform (Foster and Higham 2014), which is associated with territorial defense and courtship displays (Losos 2009).…”

A Common Endocrine Signature Marks the Convergent Evolution of an Elaborate Dance Display in Frogs

“…Thus, this work supports the hypothesis that selection drives the emergence of foot-flagging in part by enhancing the effects of androgenic steroids on certain muscle groups. Similar work in birds and lizards reveals that complex gestural displays (i.e., increased modifications to a species' display routine) appear to coevolve with dramatic increases in AR expression within select parts of the muscular system Johnson et al 2018;Schuppe and Fuxjager 2019). Functionally, these populations of AR are thought to help reshape parameters of performance, which endow individuals with novel behavioral abilities necessary for display.…”

“…This phenomenon is perhaps best studied with regard to androgenic and estrogenic sex steroids (Hau 2007;Adkins-Regan 2008;Ketterson et al 2009;McGlothlin et al 2010;Fuxjager and Schuppe 2018;Cox 2020), which mediate the reproductive morphology and behavior of most vertebrates (Adkins-Reagan 2005). For example, adaptive shifts in sexual phenotype are often associated with changes in densities of sex steroid receptors (e.g., androgen receptor [AR] and estrogen receptor) at specific sites within the nervous and musculoskeletal systems (Canoine et al 2007;Rosvall et al 2012;Bergeon Burns et al 2013;Fusani et al 2014b;Johnson et al 2018). Behavioral traits that mediate interactions among conspecifics, like sexual displays, are also sex steroid dependent (Bass 2008;Bass and Remage-Healey 2008;Zornik and Kelley 2011) and can arise convergently (Trillmich and Trillmich 1984;Ord et al 2013).…”