Yolk testosterone varies with sex in eggs of the lizard, Anolis carolinensis

Abstract

In the green anole (Anolis carolinensis), a lizard with genotypic sex determination, yolk testosterone (T) concentration is greater in male-producing than female-producing eggs at oviposition, but the source and potential effects were not clear from previous studies. If yolk T levels are also sex-specific before eggs are laid, a period during which embryonic steroidogenesis is unlikely, it would strongly suggest that the difference in yolk T is maternally derived. We collected yolk samples from eggs shelling within the oviducts of anesthetized females, and then allowed these females to lay the eggs naturally. Eggs were incubated to hatching to determine sex morphologically, and yolk T concentrations were analyzed by radioimmunoassay. As is the case just after they are laid, yolk T is higher in male than female oviductal eggs. To our knowledge, this is the earliest sex difference reported for any yolk steroid. We suggest that maternally derived yolk T levels could influence sex by differentially affecting male- and female-inducing sperm, because fertilization occurs after yolk deposition and ovulation, while the egg is in the oviduct. Our results, together with those of an increasing number of studies, suggest that a relationship between hormones and vertebrate sex determination may be more widespread than generally appreciated.

Development of the Cloaca, Hemipenes, and Hemiclitores in the Green Anole, <b><i>Anolis carolinensis</i></b>

“…Our findings indicate that sexually dimorphic development occurs early in the green anole, which supports previous findings [Winkler and Wade, 1998;Ruiz and Wade, 2002;Lovern and Wade, 2003;Lovern et al, 2004;Holmes and Wade, 2005;Beck and Wade, 2008;Cohen et al, 2012;Wade, 2012]. Development of sexually dimorphic structures, including external genitalia, in squamates has been linked to differences in sex steroid activity [Crews, 1980], and experimental studies have demonstrated the role of testosterone in sexual differentiation of anole genitalia [Winkler and Wade, 1998;Lovern et al, 2004;Beck and Wade, 2008].…”

No sex difference in yolk steroid concentrations of avian eggs at laying

“…Sex steroids do alter sex determination in reptiles with temperature-dependent sex determination (Crews 1996;Godwin & Crews 2002). Yolk steroids might play an important natural role in sex determination in those species (Janzen et al 1998;Bowden et al 2000), and possibly in reptiles with genetic sex determination as well (Lovern & Wade 2003b Yolk sex steroid levels were significantly sexually dimorphic after 10 days of incubation (MANOVA, F 4,66 Z1.07, p!0.05; note difference in y-axis scale). Standard deviations are presented to illustrate overlap in yolk steroid concentrations between the sexes.…”

“…Although these studies collected eggs before embryonic steroidogenesis is known, sex differences in sequestration or metabolism of sex steroids could occur before day 3. Furthermore, Lovern & Wade (2003b) have provided some support for the Petrie et al (2001) hypothesis, reporting sex differences in anole lizard egg yolk before significant development has taken place. Thus, the sex allocation mechanism proposed by Petrie et al (2001) continues to be influential among behavioural ecologists (e.g.…”

Follicular fluid steroid levels and subsequent sex of bovine embryos

“…There is also evidence of a hormonal influence in the adaptive control of the sex ratio in birds (Komdeur et al,'97). Lovern and Wade (2003) have moved further towards demonstrating a proximate mechanism for sex determination by showing that the testosterone level in the yolk of a lizard with genotypic sex determination is related to the sex of the offspring, with yolk testosterone concentration being greater in male-producing eggs than in female-producing eggs.…”