Female anoles retain responsiveness to testosterone despite the evolution of androgen‐mediated sexual dimorphism

Abstract

Summary1. The evolution of sexual dimorphism presents a challenge because males and females must express two phenotypes from the same underlying genome. In vertebrates, one solution to this challenge is to link the expression of shared traits to sex steroids. However, even 'male-biased' steroids such as testosterone (T) circulate at biologically significant levels in females, raising the question of whether sexual dimorphism evolves not only through the coupling of trait expression to T in males, but also through the decoupling of trait expression from T in females. 2. We tested these alternatives by asking whether male and female brown anoles (Anolis sagrei) respond to exogenous T in similar fashion with respect to a suite of sexually dimorphic traits: growth, skeletal morphology, resting metabolism, fat storage, dewlap size and dewlap colour. 3. First, we established the ontogeny of sexual dimorphism in a colony raised in a laboratory common garden. Next, we treated juveniles of each sex with either T implants or empty implants at 5-8 months of age, when sexual dimorphism first began to develop for most traits. 4. T stimulated growth in both sexes and largely abolished natural sex differences in growth. This effect was associated with the stimulation of resting metabolism and the diversion of energy from fat and liver stores in both sexes. T also enlarged the dewlap in both sexes, though females never developed dewlaps equal in size to those of males. Finally, T altered the brightness and saturation of the dewlap in both sexes, inducing coloration similar to that of adult males. 5. Female brown anoles retain many of the same tissue-specific responses to T that occur in males, suggesting that the evolution of androgen-mediated sexual dimorphism has been achieved largely through the coupling of trait expression to sex differences in circulating T, without an associated decoupling of trait expression from T in females.

Testosterone activates sexual dimorphism including male-typical carotenoid but not melanin plumage pigmentation in a female bird

“…T, DHT, E2), which may be facilitated via changes in ovarian steroid production during the pre-nuptial molt. Although a coupling of sexual dimorphism to sex differences in adult androgen secretion may explain the evolution of sex differences in many traits (Cox et al, 2015), our results implicate a role for additional actions of female hormones and non-hormonal mechanisms in regulating dimorphic expression of complex, multi-component traits.…”

Multivariate genetic architecture of the Anolis dewlap reveals both shared and sex‐specific features of a sexually dimorphic ornament

“…The reasons for this apparently general pattern of asymmetry in B are not well understood, but may include prior effects of sex‐specific selection in combination with mechanisms such as genomic imprinting, sex linkage and sex‐biased expression of the genes underlying dimorphic phenotypes (Wyman et al ., ). Although our study does not directly address any of these potential mechanisms, previous experiments have shown that dewlap size and coloration are strongly responsive to testosterone in brown anoles (Cox et al ., , ). Sex‐biased modifiers of gene expression, such as testosterone, may contribute not only to the phenotypic expression of sexual dimorphism in dewlap size and colour, but also to the corresponding reduction of between‐sex genetic correlations (Cox et al ., ) and the creation of sex‐specific patterns of phenotypic and genetic integration (i.e.…”

Ovarian control of growth and sexual size dimorphism in a male-larger gecko

“…However, the induction of male-typical growth by exogenous testosterone in non-OVX females in these two geckos (Kubicǩa et al, 2013;Starostová et al, 2013) as well as in other squamates (mostly studied in female-larger species: reviewed in Starostová et al, 2013; but also recently in the male-larger anole A. sagrei : Cox et al, 2015) still leaves open the possibility that testicular androgens can cause growth masculinization. This suggestion was based on the parsimonious expectation that elevated levels of androgens in females should have the same effect in both sexes and therefore influence growth in males and females in the same way.…”

“…However, and at first sight paradoxically, the induction of maletypical levels of circulating testosterone in females led to a 'masculinization' of growth in both female-larger and male-larger lizard species. Non-ovariectomized (non-OVX) females treated by exogenous testosterone attained larger, male-like final snout-vent length (SVL) in the male-larger lizard species (Starostová et al, 2013;Cox et al, 2015), while exogenous testosterone acted negatively on the growth and final SVL in females of the femalelarger gecko (Kubicǩa et al, 2013). We suggest that the discrepancy between the effects of testosterone in males and females can be explained by the scenario where the development of SSD does not require masculinization by male gonadal androgens, but rather feminization by female gonadal hormones.…”

“…Comparison of the growth of OVX females and OVX females treated with exogenous testosterone was carried out in order to test whether there is a direct masculinization effect of testosterone as predicted by the male androgen hypothesis, or whether the effect of exogenous testosterone on female growth in non-OVX females seen in previous experiments (e.g. Starostová et al, 2013, and citations therein;Kubicǩa et al, 2013;Cox et al, 2015) was a result of the interference of testosterone with normal ovarian function, as predicted by the ovarian hormone hypothesis. Oestrogens have been experimentally shown to be the major factor involved in bone growth control in mammals in both males and females (e.g.…”