Little evidence for switches to environmental sex determination and turnover of sex chromosomes in lacertid lizards

Abstract

Amniotes possess variability in sex determination, from environmental sex determination (ESD), where no sex chromosomes are present, to genotypic sex determination (GSD) with highly differentiated sex chromosomes. Some evolutionary scenarios postulate high stability of differentiated sex chromosomes and rare transitions from GSD to ESD. However, sex chromosome turnovers and two independent transitions from highly differentiated ZZ/ZW sex chromosomes to ESD were previously reported in the lacertid lizards. Here, we examined the homology of sex chromosomes in the wide phylogenetic spectrum of lacertids and their outgroups by comparing gene copy numbers between sexes in genes previously found to be Z-specific in some lacertids. Our current sampling covers 45 species from 26 genera including lineages supposed to possess a derived sex determining systems. We found that all tested lacertids share homologous differentiated ZZ/ZW sex chromosomes, which were present already in their common ancestor living around 85 million years ago. These differentiated sex chromosomes are not present in amphisbaenians and teiid lizards, the close relatives of lacertids. Our study demonstrates how inaccuracies in data can influence the outcome of phylogenetic reconstructions of evolution of sex determination, in this case they overestimated the number of shifts from GSD to ESD and the rate in turnovers of sex chromosomes.

Chromosome Painting Does Not Support a Sex Chromosome Turnover in Lacerta agilis Linnaeus, 1758

“…Later, Rovatsos et al [2016Rovatsos et al [ , 2019c used transcriptome analysis and qPCR to identify hemizygous, and thus suggestively Z-linked, genes in several species of lacertids, including L. agilis from the Czech Republic ( L. agilis argus ). In these studies, the genes reported as Z-specific by Srikulnath et al [2014] were identified as (pseudo)autosomal.…”

“…In these studies, the genes reported as Z-specific by Srikulnath et al [2014] were identified as (pseudo)autosomal. The orthologues of the Z-linked genes which were determined by Rovatsos et al [2016Rovatsos et al [ , 2019c are located in 2 microchromosomes of A. carolinensis , ACA11 and ACA16 (homologous to GGA4p and GGA17, respectively) [Kichigin et al, 2016]. Rovatsos et al suggested that the Z chromosome of lacertids should be one of the small macrochromosomes, formed via fusion of 2 ancestral squamate microchromosomes [Uno et al, 2012].…”

Chromosome painting does not support a sex chromosome turnover in Lacerta agilis Linnaeus, 1758

“…3a). The absence of the signal on the W chromosome is apparently due to the fact that the W chromosome of lacertids is too degenerated and does not hybridize with the DNA from the Z chromosome [Rovatsos et al, 2019b; Andrade et al, 2019]. The autosomes were identified as pairs 13 and 14 basing on the position of the LST_L peak in the flow karyotype.…”

“…Later, Rovatsos et al [2016; 2019b] used transcriptome analysis and qPCR to identify hemizygous and thus suggestively Z-linked genes in several species of lacertids, including L. agilis from the Czech Republic ( L. agilis argus ). In these works, the genes identified by Srikulnath et al [2014] as Z-specific were identified as (pseudo)autosomal.…”

“…In these works, the genes identified by Srikulnath et al [2014] as Z-specific were identified as (pseudo)autosomal. The homeologues of the Z-linked genes which were identified by Rovatsos et al [2016, 2019b] are located in two microchromosomes of A. carolinensis : ACA11 and ACA16 (homologous to GGA4p and GGA17, respectively) [Kichigin et al, 2016]. The authors suggested that the Z chromosome of lacertids should be one of the small macrochromosomes, formed via fusion of two ancestral squamate microchromosomes [Uno et al, 2012].…”