Independent Evolution of Sex Chromosomes in Eublepharid Geckos, A Lineage with Environmental and Genotypic Sex Determination

Abstract

Geckos demonstrate a remarkable variability in sex determination systems, but our limited knowledge prohibits accurate conclusions on the evolution of sex determination in this group. Eyelid geckos (Eublepharidae) are of particular interest, as they encompass species with both environmental and genotypic sex determination. We identified for the first time the X-specific gene content in the Yucatán banded gecko, Coleonyx elegans, possessing X1X1X2X2/X1X2Y multiple sex chromosomes by comparative genome coverage analysis between sexes. The X-specific gene content of Coleonyx elegans was revealed to be partially homologous to genomic regions linked to the chicken autosomes 1, 6 and 11. A qPCR-based test was applied to validate a subset of X-specific genes by comparing the difference in gene copy numbers between sexes, and to explore the homology of sex chromosomes across eleven eublepharid, two phyllodactylid and one sphaerodactylid species. Homologous sex chromosomes are shared between Coleonyx elegans and Coleonyx mitratus, two species diverged approximately 34 million years ago, but not with other tested species. As far as we know, the X-specific gene content of Coleonyx elegans / Coleonyx mitratus was never involved in the sex chromosomes of other gecko lineages, indicating that the sex chromosomes in this clade of eublepharid geckos evolved independently.

Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation

“…The X-linked genes from the region homologous to a part of PMU10 have homologues linked to a region of chicken chromosome 1 (GGA1). As far as is known, the PMU10/ GGA1 syntenic block is among amniotes involved in sex chromosomes only in skinks and the phylogenetically distant geckos from the genus Coleonyx [22,53] supporting the hypothesis that the sex chromosomes in skinks evolved independently from other amniote sex chromosomes. Notably, this chromosomal region contains several genes, which are involved in gonad development or in pathological conditions (dmc1, ep300, igf1, kitlg, nup107, pdgfb, sbf1, sox10, stra8, sycp3) and can potentially act as the sex-determining gene(s) in skinks.…”

Sex chromosome evolution among amniotes: is the origin of sex chromosomes non-random?

“…Corrections of these inaccuracies together with the recent reports of sex determination in previously unstudied lineages (electronic supplementary material, table 1) such as Gila monsters and beaded lizards [43,44], xantusiids [45] and several lineages of geckos [46][47][48][49] and skinks [12] led to a hopefully more reliable dataset to reconstruct the evolutionary history of sex determination in amniotes. We should keep in mind that we have more or less reliable direct data on sex determination in likely less than 5% out of roughly 11 000 current species of non-avian reptiles [47].…”

Lizards as Model Organisms of Sex Chromosome Evolution: What We Really Know from a Systematic Distribution of Available Data?

“…The opposite hypothesis of ancestral GSD in amniotes cannot be rejected basing on available evidence, but it would require a much higher number of transitions, resulting evolutionary less parsimonious [ 77 ]. Furthermore, GSD in amniotes, and particularly in lizards, includes a number of different systems which followed distinct evolutionary pathways, involving non-homologous chromosome pairs [ 5 , 14 , 78 , 79 ].…”

“…For example, the conserved ZW pair in birds shows no homology with the XY of mammals or the snake ZW pair [ 135 , 136 ]. Non-homology of sex chromosomes has been demonstrated also between most main lizard evolutionary lineages, as well as within families showing sex chromosome turnover and multiple shifts between GSD and TSD (e.g., References [ 14 , 15 , 78 , 132 ]). Nevertheless, recent studies highlighted the occurrence of partial homologies between the Z chromosome of Gekko hokouensis , the avian Z chromosome, the X chromosome of giant musk turtles of the genus Staurotypus .…”

“…The growing interest in lizard sex determination and sex chromosome systems produced in recent years a sensible increase of the available data on different taxonomic groups (e.g., References [ 12 , 13 , 14 , 15 , 16 , 17 ]), which might be useful to provide novel insights on the phylogenetic distribution of different systems.…”