Evolution of sex chromosomes in Sauropsida

Abstract

Reptiles (sauropsids) represent the sister group to mammals, and the basal members of Reptilia may provide a good model for the condition of the common ancestor of both groups. Sex-determining mechanisms (SDM) and organizations of sex chromosomes among genotypically sex-determining (GSD) species vary widely across reptiles. Birds and snakes, for example, are entirely GSD whereas other reptiles, like all crocodilians, exhibit temperature-dependent sex determination (TSD). Here we explore the evolution of sex chromosomes and SDM within reptiles, using family-level analyses of character evolution and applying parsimony, likelihood, Bayesian, and stochastic methods. We find support for the common ancestor of amphisbaenians and whiptail lizards (Laterata) possessing the XY (male heterogametic) GSD mechanism, while the ancestors of Testudines and Crocodylia, as well as the larger group Archosauromorpha (here containing turtles) are inferred to have exhibited TSD. We also find evidence consistent with the hypothesis that the XY system is more labile and evolves faster than does the ZW (female heterogametic) system. Phylogenetic-based speciation tests do not support an association between GSD and speciation, and reject the hypothesis that the presence of the XY system is associated with speciation in reptiles.

Fig. 1

Parsimony reconstruction with sex determination coded as a polymorphic variable across many families of reptiles. Mammals and amphibians are represented at the species level. (A) Parsimony reconstruction of sex determination coded as a binary variable takes 14 steps and is equivocal concerning the ancestral family-level condition of sex determination in the deepest nodes within Sauropsida, but reconstructs Squamata as genotypic sex determination. (B) Parsimony reconstruction of sex determination coded as a multistate variable takes 21 steps and is equivocal concerning the ancestral family-level condition of sex determination in the deepest nodes within Sauropsida, but reconstructs Lacertilia as having an XY system and Archosauromorpha as having temperature-dependent sex determination.

Fig. 2

Bayesian posterior-probability fraction of sex determination coded as a multistate character for the family-level ancestor in several important nodes of the sauropsid tree. “*+” indicates significant support for the designated type of sex determination while “*−” indicates significant rejection (two of the three pair-wise comparisons rejected).