Differences in Homomorphic Sex Chromosomes Are Associated with Population Divergence in Sex Determination in Carinascincus ocellatus (Scincidae: Lygosominae)

Abstract

Sex determination directs development as male or female in sexually reproducing organisms. Evolutionary transitions in sex determination have occurred frequently, suggesting simple mechanisms behind the transitions, yet their detail remains elusive. Here we explore the links between mechanisms of transitions in sex determination and sex chromosome evolution at both recent and deeper temporal scales (<1 Myr; ~79 Myr). We studied a rare example of a species with intraspecific variation in sex determination, Carinascincus ocellatus, and a relative, Liopholis whitii, using c-banding and mapping of repeat motifs and a custom Y chromosome probe set to identify the sex chromosomes. We identified both unique and conserved regions of the Y chromosome among C. ocellatus populations differing in sex determination. There was no evidence for homology of sex chromosomes between C. ocellatus and L. whitii, suggesting independent evolutionary origins. We discuss sex chromosome homology between members of the subfamily Lygosominae and propose links between sex chromosome evolution, sex determination transitions, and karyotype evolution.

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

“…From a cytogenetic point of view, the evolution of differentiated sex chromosomes begins from homomorphic autosomal ancestors, after the insurgence of a sex-determining allele [85,86]. Studies on neo-formed sex chromosomes show that they are mostly pseudoautosomal, homomorphic and often undetectable with standard karyotyping (e.g., References [87,88]). The progressive diversification of the Y/W element may be promoted by the accumulation and fixation of deleterious mutations and recombination suppression in the region containing the sex-determining allele [89][90][91][92].…”

“…In general, the different steps and pathways of sex chromosome evolution here described ( Figure 1 ) do not follow a common timeframe. Heterogametic chromosomes may quickly diversify and degenerate in some lineages, while they persist over a long evolutionary period of time in other groups as poorly differentiated elements [ 8 , 16 , 71 , 76 , 88 ].…”

“…In some cases (e.g., Norops, Dactyloidae, Sceloporus and Phrynosomatidae), fusions between autosomes and sex chromosomes, rather than producing multiple sex chromosome systems may generate single, albeit enlarged pairs, containing distinct pseudoautosomal regions [ 116 , 117 , 118 ]. In rare cases, sex chromosome diversification can be observed also at intraspecific level in lizards, as in the case of Carinascincus ocellatus, where ecologically distinct populations exhibit different heterochromatinization levels of the Y chromosome [ 88 ]. However, poorly differentiated but highly conserved XY chromosomes generally characterize the family Scincidae.…”

Cytogenetically Elusive Sex Chromosomes in Scincoidean Lizards

“…The scincoidean lizards have been examined cytogenetically for decades, but sex chromosomes were reported only rarely. XX/XY sex chromosomes have been identified in a few skink species by C-banding, silver-staining, fluorescence in situ hybridization (FISH) with repetitive elements and rDNA loci, or by size differences between X and Y [7,[13][14][15]. Heteromorphic XX/XY sex chromosomes were documented in Oligosoma oliveri [13; reported there as Cyclodina oliveri], Saproscincus czechurai, Lampropholis sp.…”

“…The high age of the XX/XY sex determination system in skinks was independently supported by the analysis of the divergence of gametologs [25]. Recently, a Y-specific probe was designed from Illumina reads, derived from double-digest restriction-site associated DNA sequencing (ddRADseq), which accurately revealed the Y chromosome in the skink Carinascincus ocellatus, but not in the closely related Liopholis whitii [15]. Notably, heteromorphic ZZ/ZW sex chromosomes have been identified by conventional staining in the skink Scincella melanosticta [23], which would represent a rare case of sex chromosome turnover among skinks.…”