It’s a Trap?! Escape from an ancient, ancestral sex chromosome system and implication ofFoxl2as the putative primary sex determining gene in a lizard (Anguimorpha; Shinisauridae)

Abstract

Although sex determination is ubiquitous in vertebrates, mechanisms of sex determination vary from environmentally- to genetically-influenced. Genetic sex determination is typically accomplished with sex chromosomes via the presence/absence of a specific allele at a genetic locus, which initiates the sex determination signaling network. In vertebrates, well-studied groups like mammals and birds maintain conserved sex chromosome systems (XY and ZW, respectively), while sex chromosomes in many other clades may not be conserved across long evolutionary timeframes. Among squamate reptiles, for example, some groups are relatively stable, like iguanids (Pleurodonta), caenophidian snakes (Caenophidia), and lacertids (Lacertidae) while others are highly variable in their modes of sex determination, such as geckos (Gekkota) and the clade containing chameleons and dragon lizards (Acrodonta). One group inferred to have an evolutionarily stable mode of sex determination is the Anguimorpha, a clade of charismatic taxa, including monitor lizards (Varanus), beaded lizards (Heloderma), glass lizards (Ophisaurus), and the crocodile lizard (Shinisaurus crocodilurus). The most recent common ancestor to extant anguimorphs possessed a ZW system that has been retained across the clade. However, determination of sex chromosomes in some anguimorph species has remained elusive including in the endangered, monotypic family of crocodile lizards (Shinisauridae). Here, we use a combination of whole genome re-sequencing and RADseq to demonstrate that S. crocodilurus has replaced the ancestral anguimorph ZW system on their LG7 chromosome with a novel ZW system on LG3. The syntenic region that corresponds with this linkage group in chicken is chromosome 9, and this is the first documented use of this syntenic block as a sex chromosome in amniotes. Additionally, this ~1Mb region harbors approximately 10 genes, including a duplication of the well-characterized transcription factor, Foxl2, a critical locus for the maintenance of sexual differentiation in vertebrates, and thus a putative primary sex determining gene for S. crocodilurus.