Embryonic temperature and gonadal sex organize male-typical sexual and aggressive behavior in a lizard with temperature-dependent sex determination

Abstract

Temperature during embryonic development determines gonadal sex in the leopard gecko, Eublepharis macularius. Moreover, both embryonic temperature and gonadal sex influence adult behavior. Yet it remains unclear whether the effects of embryonic temperature and gonadal sex on behavior are irreversibly organized during development. To address this question, we gonadectomized adult females and males generated from a temperature that produces mostly females (30 C) and a temperature that produces mostly males (32.5 C). Females and males from both temperatures were then treated with equivalent levels of various sex steroids. We found that both embryonic temperature and gonadal sex had persistent effects on the expression of male-typical sexual and aggressive behaviors. For example, adult females do not scent mark and display very little courtship and mounting behavior even when treated with levels of hormones (primarily androgens) that activate these behaviors in males. In contrast, species-typical aggressive displays were less sex specific and were activated by both dihydrotestosterone and testosterone (T) in males and by T in females. Nevertheless, the average duration of aggressive displays was significantly shorter in T-treated females than that in T-treated males. With regard to submissive behavior, androgens decreased flight behavior in males, but had no effect in females. Embryonic temperature had enduring effects on certain behaviors in males. For instance, males from a male-biased embryonic temperature scent-marked more than males from a female-biased embryonic temperature when treated with dihydrotestosterone or T. Conversely, and across hormone treatments, males from a female-biased embryonic temperature mounted more than males from a male-biased embryonic temperature. Finally, treatment with 17beta-estradiol decreased submissive behavior in males from a male-biased embryonic temperature compared with that in males from a female-biased embryonic temperature. Courtship and aggressive behavior were not influenced by temperature. These results strongly suggest that male-typical behaviors in the adult leopard gecko are permanently organized by both embryonic temperature and gonadal sex during development.