Testosterone, growth and the evolution of sexual size dimorphism

Abstract

The integration of macroevolutionary pattern with developmental mechanism presents an outstanding challenge for studies of phenotypic evolution. Here, we use a combination of experimental and comparative data to test whether evolutionary shifts in the direction of sexual size dimorphism (SSD) correspond to underlying changes in the endocrine regulation of growth. First, we combine captive breeding studies with mark‐recapture data to show that male‐biased SSD develops in the brown anole lizard (Anolis sagrei) because males grow significantly faster than females as juveniles and adults. We then use castration surgeries and testosterone implants to show that castration inhibits, and testosterone stimulates, male growth. We conclude by reviewing published testosterone manipulations in other squamate reptiles in the context of evolutionary patterns in SSD. Collectively, these studies reveal that the evolution of SSD has been accompanied by underlying changes in the effect of testosterone on male growth, potentially facilitating the rapid evolution of SSD.

Neither male gonadal androgens nor female reproductive costs drive development of sexual size dimorphism in lizards

“…The Journal of Experimental Biology 216 (10) et al (Cox et al, 2009) and other resources not included in their study (Civantos, 2002;Duncan, 2011;Kubička et al, 2013), we conclude that the support for the hypothesis that gonadal androgens directly influence the endocrine growth axis in squamate reptiles is not very strong. We suggest that previously reported effects of gonadal androgens on growth in male lizards could be attributed either to unnatural levels of testosterone, or to indirect consequences of altered behaviour or social status in manipulated individuals (see also Cox et al, 2006).…”

“…In their review, Cox and colleagues (their table2) concluded that regardless of phylogenetic distribution, androgens enhance male growth in male-larger species, inhibit it in female-larger species, but have ambiguous or no obvious effect in species that are monomorphic in body size (Cox et al, 2009). They speculated that this bipotential effect of testosterone on growth could involve direct effects on the endocrine growth axis.…”

“…The replacement of exogenous testosterone in castrated males is used to test whether the observed effects of castration are caused by eliminating the primary source of testosterone versus other functions of the testes. In two of the reviewed studies (Cox et al, 2009;Kubička et al, 2013), castration alone did not have any significant effect on male growth in comparison to control males, but administration of exogenous testosterone significantly influenced growth of castrated males. These results suggest that artificial hormone delivery, via implanted Silastic tubules, might fail to faithfully replicate natural in vivo patterns of gonadal secretion.…”

“…Based on results of hormonal manipulations in species from the iguanian genus Sceloporus with opposite SSD patterns, they proposed that testosterone can have positive effects on male growth in male-larger species but negative effects on male growth in female-larger species. Cox and colleagues (Cox et al, 2009) expanded the test of this hypothesis by conducting experimental work in another iguanian species (Anolis sagrei) and performing phylogenetically informed analysis of previously published results of hormonal manipulations in squamate reptiles. In their review, they reported that androgens enhance male growth in male-larger species, inhibit it in female-larger species, but have ambiguous or no obvious effect in species that are monomorphic in body size.…”

Age estimation through skeletochronology and mark-recapture of free-living Liolaemus leopardinus (Squamata: Liolaemidae) from Chile

“…Thus, we suggest that adult males may live longer than adult females, since reptiles generally show indeterminate growth. If so, the longer lifespan in males might have a genetic basis (Badyaev 2002, Cox et al 2009, Barret and Richardson 2011 since males do not defend territories or females, and do not engage in agonistic behavior against male conspecifics (Fox and Shipman 2003, ESB pers. observ.…”