Evolutionary stability of sex chromosomes in snakes

Abstract

Amniote vertebrates possess various mechanisms of sex determination, but their variability is not equally distributed. The large evolutionary stability of sex chromosomes in viviparous mammals and birds was believed to be connected with their endothermy. However, some ectotherm lineages seem to be comparably conserved in sex determination, but previously there was a lack of molecular evidence to confirm this. Here, we document a stability of sex chromosomes in advanced snakes based on the testing of Z-specificity of genes using quantitative PCR (qPCR) across 37 snake species (our qPCR technique is suitable for molecular sexing in potentially all advanced snakes). We discovered that at least part of sex chromosomes is homologous across all families of caenophidian snakes (Acrochordidae, Xenodermatidae, Pareatidae, Viperidae, Homalopsidae, Colubridae, Elapidae and Lamprophiidae). The emergence of differentiated sex chromosomes can be dated back to about 60 Ma and preceded the extensive diversification of advanced snakes, the group with more than 3000 species. The Z-specific genes of caenophidian snakes are (pseudo)autosomal in the members of the snake families Pythonidae, Xenopeltidae, Boidae, Erycidae and Sanziniidae, as well as in outgroups with differentiated sex chromosomes such as monitor lizards, iguanas and chameleons. Along with iguanas, advanced snakes are therefore another example of ectothermic amniotes with a long-term stability of sex chromosomes comparable with endotherms.

Keywords: evolution; reptiles; sex chromosomes; sex determination; snakes.

Figure 1.

Relative gene dose ratios between a female and a male in 42 species of snakes (A) and lizard outgroups (B, Iguania; C, Anguimorpha). Values (means + s.d.) are depicted in red for the snake Z-linked genes, for (pseudo)autosomal loci homologous to ACA6 in yellow and for the control autosomal locus in blue. Value 1.0 is expected for autosomal or pseudoautosomal genes, while value 0.5 is consistent with Z-linkage. Our results suggest that sex chromosomes are highly differentiated and homologous across all caenophidian snakes. In contrast, the Z-specific genes of caenophidian snakes are pseudoautosomal or autosomal in non-caenophidian snakes and snake outgroups. (Online version in colour.)