Molecular evolution of Dmrt1 accompanies change of sex-determining mechanisms in reptilia

Abstract

In reptiles, sex-determining mechanisms have evolved repeatedly and reversibly between genotypic and temperature-dependent sex determination. The gene Dmrt1 directs male determination in chicken (and presumably other birds), and regulates sex differentiation in animals as distantly related as fruit flies, nematodes and humans. Here, we show a consistent molecular difference in Dmrt1 between reptiles with genotypic and temperature-dependent sex determination. Among 34 non-avian reptiles, a convergently evolved pair of amino acids encoded by sequence within exon 2 near the DM-binding domain of Dmrt1 distinguishes species with either type of sex determination. We suggest that this amino acid shift accompanied the evolution of genotypic sex determination from an ancestral condition of temperature-dependent sex determination at least three times among reptiles, as evident in turtles, birds and squamates. This novel hypothesis describes the evolution of sex-determining mechanisms as turnover events accompanied by one or two small mutations.

Keywords: ancestral reconstruction; archosaur; convergence; sex determination; squamate.

Figure 1.

Maximum-likelihood analysis of an ancestral Dmrt1 protein for diapsids, archosaurs and lepidosaurs. A consistent amino acid shift at positions 54 and 57 in the alignment largely distinguishes GSD and TSD species. Most TSD species (bold Latin binomials) have T and S in positions 54 and 57 of this sequence, suggesting mutation at these positions in the gene that codes for Dmrt1 accompanies a change in sex-determining mechanism. Grey outlined columns indicate positions 54 and 57. Bold amino acids indicate species with the T54–S57 amino acid state. The set of states at each node is ordered from most to least likely, excluding states with probabilities below 5%. Amino acid states in parentheses are ambiguous.