The Adaptive Significance of Temperature-Dependent Sex Determination: Experimental Tests With a Short-Lived Lizard

Abstract

Why is the sex of many reptiles determined by the temperatures that these animals experience during embryogenesis, rather than by their genes? The Charnov-Bull model suggests that temperature-dependent sex determination (TSD) can enhance maternal fitness relative to genotypic sex determination (GSD) if offspring traits affect fitness differently for sons versus daughters and nest temperatures either determine or predict those offspring traits. Although potential pathways for such effects have attracted much speculation, empirical tests largely have been precluded by logistical constraints (i.e., long life spans and late maturation of most TSD reptiles). We experimentally tested four differential fitness models within the Charnov-Bull framework, using a short-lived, early-maturing Australian lizard (Amphibolurus muricatus) with TSD. Eggs from wild-caught females were incubated at a range of thermal regimes, and the resultant hatchlings raised in large outdoor enclosures. We applied an aromatase inhibitor to half the eggs to override thermal effects on sex determination, thus decoupling sex and incubation temperature. Based on relationships between incubation temperatures, hatching dates, morphology, growth, and survival of hatchlings in their first season, we were able to reject three of the four differential fitness models. First, matching offspring sex to egg size was not plausible because the relationship between egg (offspring) size and fitness was similar in the two sexes. Second, sex differences in optimal incubation temperatures were not evident, because (1) although incubation temperature influenced offspring phenotypes and growth, it did so in similar ways in sons versus daughters, and (2) the relationship between phenotypic traits and fitness was similar in the two sexes, at least during preadult life. We were unable to reject a fourth model, in which TSD enhances offspring fitness by generating seasonal shifts in offspring sex ratio: that is, TSD allows overproduction of daughters (the sex likely to benefit most from early hatching) early in the nesting season. In keeping with this model, hatching early in the season massively enhanced body size at the beginning of the first winter, albeit with a significant decline in probability of survival. Thus, the timing of hatching is likely to influence reproductive success in this short-lived, early maturing species; and this effect may well differ between the sexes.

Exogenous application of estradiol to eggs unexpectedly induces male development in two turtle species with temperature-dependent sex determination

“…In addition, Fadrozole has previously been shown to induce male development by blocking the aromatization of androgens to estrogens in many taxa (Piferrer et al, 1994;Wibbels and Crews, 1994;Chardard and Dournon, 1999;Warner et al, 2005). Intriguingly, our results in two turtle species across four independent experiments are inconsistent with 13 these well-established findings; the application of Fadrozole had no impact on offspring sex ratios in the present study, and applying estradiol to eggs produced nearly all male offspring, a pattern opposite of expectations.…”

“…Indeed, in 2008 the Fadrozole used was obtained five years earlier and worked effectively at that time (see Warner and Shine, 2005). Because of this concern, fresh Fadrozole was obtained in 2010, and still produced the same results (i.e., no effect of Fadrozole on sex determination).…”

Extension, single-locus conversion and physical mapping of sex chromosome sequences identify the Z microchromosome and pseudo-autosomal region in a dragon lizard, Pogona vitticeps

“…This is true even within the family of dragon lizards (Agamidae), which are emerging as a model group for the study of sex determination evolution, sex ratio evolution and sex allocation (Harlow, 2004;Ezaz et al, 2005;Warner and Shine, 2005;Doody et al, 2006;Janzen and Phillips, 2006;Quinn et al, 2007;Shine, 2007, 2008;Ezaz et al, 2009). They present an excellent opportunity to understand better the molecular and chromosomal basis of evolutionary transitions between the two fundamental mechanisms of vertebrate sex determination, TSD and GSD.…”

No Seasonal Sex-Ratio Shift Despite Sex-Specific Fitness Returns of Hatching Date in a Lizard With Genotypic Sex Determination

“…For example, sex-specific fitness in relation to hatching or parturition date is believed to be the underlying cause for the evolution of temperaturedependent sex determination (TSD) in short-lived species (Shine 1999;Warner and Shine 2005). Temperature could act as an adaptive sex determining factor if it is related to developmental time and therefore date of hatching, or if thermal incubation conditions differ predictably over the season (Shine 1999;Wapstra et al 2004;Warner and Shine 2005). Thus, strong selection for seasonal sex-ratio shifts could partly explain the repeated evolution of TSD in short-lived Australian agamids (Harlow 2004;Warner and Shine 2005).…”