Segregating variation for temperature-dependent sex determination in a lizard

Abstract

Temperature-dependent sex determination (TSD) was first reported in 1966 in an African lizard. It has since been shown that TSD occurs in some fish, several lizards, tuataras, numerous turtles and all crocodilians. Extreme temperatures can also cause sex reversal in several amphibians and lizards with genotypic sex determination. Research in TSD species indicates that estrogen signaling is important for ovary development and that orthologs of mammalian genes have a function in gonad differentiation. Nevertheless, the mechanism that actually transduces temperature into a biological signal for ovary versus testis development is not known in any species. Classical genetics could be used to identify the loci underlying TSD, but only if there is segregating variation for TSD. Here, we use the 'animal model' to analyze inheritance of sexual phenotype in a 13-generation pedigree of captive leopard geckos, Eublepharis macularius, a TSD reptile. We directly show genetic variance and genotype-by-temperature interactions for sex determination. Additive genetic variation was significant at a temperature that produces a female-biased sex ratio (30°C), but not at a temperature that produces a male-biased sex ratio (32.5°C). Conversely, dominance variance was significant at the male-biased temperature (32.5°C), but not at the female-biased temperature (30°C). Non-genetic maternal effects on sex determination were negligible in comparison with additive genetic variance, dominance variance and the primary effect of temperature. These data show for the first time that there is segregating variation for TSD in a reptile and consequently that a quantitative trait locus analysis would be practicable for identifying the genes underlying TSD.

Figure 1

Sex ratio as a function of incubation temperature and breeding season in leopard geckos.

Figure 2

Sex ratio reaction norms as a function of incubation temperature and family identity in leopard geckos. Each line connects the sex ratio for an individual half-sib family (that is offspring sired by a single male) that was divided between two incubation temperatures as described in the text.

Figure 3

Hypothetical model for temperature-dependent allelic effects on sex ratio at 30 and 32.5 °C. Although the S_M and S_F alleles have additive effects on sex ratio at 30 °C, the S_M allele displays dominance at 32.5 °C. This model could explain the observed pattern of genotype–environment interactions and environment-specific heritability/dominance.