Whole-chromosome fusions in the karyotype evolution ofSceloporus(Iguania, Reptilia) are more frequent in sex chromosomes than autosomes

Abstract

Whole-chromosome fusions play a major role in the karyotypic evolution of reptiles. It has been suggested that certain chromosomes tend to fuse with sex chromosomes more frequently than others. However, the comparative genomic synteny data are too scarce to draw strong conclusions. We obtained and sequenced chromosome-specific DNA pools of Sceloporus malachiticus , an iguanian species which has experienced many chromosome fusions. We found that four of seven lineage-specific fusions involved sex chromosomes, and that certain syntenic blocks which constitute the sex chromosomes, such as the homologues of the Anolis carolinensis chromosomes 11 and 16, are repeatedly involved in sex chromosome formation in different squamate species. To test the hypothesis that the karyotypic shift could be associated with changes in recombination patterns, we performed a synaptonemal complex analysis in this species and in Sceloporus variabilis (2 n = 34). It revealed that the sex chromosomes in S. malachiticus had two distal pseudoautosomal regions and a medial differentiated region. We found that multiple fusions little affected the recombination rate in S. malachiticus . Our data confirm more frequent involvement of certain chromosomes in sex chromosome formation, but do not reveal a connection between the gonosome–autosome fusions and the evolution of recombination rate. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

“…Non-random fusions can, however, be explained by the close physical proximity of particular chromosomes in the nucleus, as recently supported by the analyses of the multiple neo-sex chromosomes formation in platypus [178]. In fact, new data in iguanas [177] confirm more frequent involvement of certain chromosomes in sex chromosome formation, but at the same time do not reveal a connection between the sex chromosome-autosome fusions and the evolution of recombination rate, which would be important for a role of sex chromosomes in the resolution of intralocus sexual conflict. The reasons for the non-random fusion of certain genomic parts to sex chromosomes should be explored in the future, using comparative data.…”

“…sex-specific expression) to transition to a sex chromosome. On the other hand, the hypothesis that sexual antagonism can favour the location of a sex-determining gene in a region enriched by genes with sexually antagonistic effects received support by non-random fusions of certain autosomes with sex chromosomes in iguanas [177] and songbirds [139]. Particularly in songbirds, one region fused to the ancestral ZZ/ZW was found to be enriched in genes with predicted sex-related functions [139].…”

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

“…Single-chromosome sequencing (ChromSeq) is a further promising method in the study of sex chromosome system. By combining chromosome isolation (via microdissection or flow sorting), whole-genome amplification (WGA), hybridization and bioinformatic techniques ChromSeq has the power to the gap between cytogenetic and genomic studies [ 116 , 117 , 118 ]. So far, ChromSeq has been performed on just a handful of lizard species, but its application on a wider selection of taxa would help to uncover poorly study features of the lizard genome and karyotype [ 116 , 117 , 118 ].…”

“…In these clades, repeated fusions between the Y chromosome and non-homologous autosomes have been identified in different closely related lineages, further promoting their high karyological variability [ 71 ]. 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 ].…”

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

“…We still have only limited information about identity and location of sex-determining genes and content of parts newly added to sex chromosomes. Emerging evidence in birds, monotremes and lizards suggests more frequent involvement of certain chromosomes in neo-sex chromosome formations [21,101,121,122]. Particularly multiple neo-sex chromosomes formed by a fusion of an autosome with a Y chromosome evolved many times in amniotes, e.g.…”