Evolutionary stability of sex chromosomes in snakes

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.     

What was the ancestral sex‐determining mechanism in amniote vertebrates?

Amniote vertebrates, the group consisting of mammals and reptiles including birds, possess various mechanisms of sex determination. Under environmental sex determination (ESD), the sex of individuals depends on the environmental conditions occurring during their development and therefore there are no sexual differences present in their genotypes. Alternatively, through the mode of genotypic sex determination (GSD), sex is determined by a sex‐specific genotype, i.e. by the combination of sex chromosomes at various stages of differentiation at conception. As well as influencing sex determination, sex‐specific parts of genomes may, and often do, develop specific reproductive or ecological roles in their bearers. Accordingly, an individual with a mismatch between phenotypic (gonadal) and genotypic sex, for example an individual sex‐reversed by environmental effects, should have a lower fitness due to the lack of specialized, sex‐specific parts of their genome. In this case, evolutionary transitions from GSD to ESD should be less likely than transitions in the opposite direction. This prediction contrasts with the view that GSD was the ancestral sex‐determining mechanism for amniote vertebrates. Ancestral GSD would require several transitions from GSD to ESD associated with an independent dedifferentiation of sex chromosomes, at least in the ancestors of crocodiles, turtles, and lepidosaurs (tuataras and squamate reptiles). In this review, we argue that the alternative theory postulating ESD as ancestral in amniotes is more parsimonious and is largely concordant with the theoretical expectations and current knowledge of the phylogenetic distribution and homology of sex‐determining mechanisms.     

Sex-linked markers and microsatellite locus duplication in the cichlid species Oreochromis tanganicae

Cichlid species of the genus Oreochromis vary in their genetic sex-determination systems. In this study, we used microsatellite DNA markers to characterize the sex-determination system in Oreochromis tanganicae. Markers on linkage group 3 were associated with phenotypic sex, with an inheritance pattern typical of a female heterogametic species (WZ-ZZ). Further, locus duplication was observed for two separate microsatellite markers on the sex chromosome. These results further advance our understanding of the rapidly evolving sex-determination systems among these closely related tilapia species.     

早期胚胎的发育选择:性别决定

性别决定是一个复杂的发育调控过程, 早期胚胎发育过程中, 雌雄二者必居其一的发育选择是胚胎性腺形成必须的发育决定。文章综述了动物性别决定的遗传系统、性腺发生、性别决定关键基因及其作用机制, 从分子进化的角度分析了性染色体与性别决定形成机制, 提示性别决定基因在进化中总是趋向异配性染色体。     

Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard

An individual's sex depends upon its genes (genotypic sex determination or GSD) in birds and mammals, but reptiles are more complex: some species have GSD whereas in others, nest temperatures determine offspring sex (temperature-dependent sex determination). Previous studies suggested that montane scincid lizards (Bassiana duperreyi, Scincidae) possess both of these systems simultaneously: offspring sex is determined by heteromorphic sex chromosomes (XX-XY system) in most natural nests, but sex ratio shifts suggest that temperatures override chromosomal sex in cool nests to generate phenotypically male offspring even from XX eggs. We now provide direct evidence that incubation temperatures can sex-reverse genotypically female offspring, using a DNA sex marker. Application of exogenous hormone to eggs also can sex-reverse offspring (oestradiol application produces XY as well as XX females). In conjunction with recent work on a distantly related lizard taxon, our study challenges the notion of a fundamental dichotomy between genetic and thermally determined sex determination, and hence the validity of current classification schemes for sex-determining systems in reptiles.     

A supernumerary “B-sex” chromosome drives male sex determination in the Pachón cavefish,Astyanax mexicanus

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Nest-site philopatry and selection for environmental sex determination

The reason for the frequent occurrence of environmental sex determination (ESD) in reptiles is still not well understood, although much effort has been devoted to solving the issue. Stimulated by the occurrence of nest-site philopatry in some species, this paper examines a diploid model of the influence of nest-site philopatry on the evolution of ESD. Analysis shows that nest-site philopatry can lead to ESD because the fitnesses of sons and daughters are not influenced in the same way by nest-site quality. Daughters inherit the nest site and thus benefit more than sons from a high-quality nest site. Conversely, the fitness of daughters at low-quality nest sites is lower compared to the fitness of sons. Therefore, genes causing ESD can spread by causing the production of more sons at low-quality nest sites and more daughters at high-quality nest sites. Suggestions are made to test empirically whether nest-site philopatry led to the evolution of ESD. This revised version was published online in July 2006 with corrections to the Cover Date.     

Does the speciation clock tick more slowly in the absence of heteromorphic sex chromosomes?

Squamates may be an attractive group in which to study the influence of sex chromosomes on speciation rates because of the repeated evolution of heterogamety (both XY and ZW), as well as an apparently large number of taxa with environmental sex-determination.