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

Abstract

Sex chromosomes are a great example of a convergent evolution at the genomic level, having evolved dozens of times just within amniotes. An intriguing question is whether this repeated evolution was random, or whether some ancestral syntenic blocks have significantly higher chance to be co-opted for the role of sex chromosomes owing to their gene content related to gonad development. Here, we summarize current knowledge on the evolutionary history of sex determination and sex chromosomes in amniotes and evaluate the hypothesis of non-random emergence of sex chromosomes. The current data on the origin of sex chromosomes in amniotes suggest that their evolution is indeed non-random. However, this non-random pattern is not very strong, and many syntenic blocks representing putatively independently evolved sex chromosomes are unique. Still, repeatedly co-opted chromosomes are an excellent model system, as independent co-option of the same genomic region for the role of sex chromosome offers a great opportunity for testing evolutionary scenarios on the sex chromosome evolution under the explicit control for the genomic background and gene identity. Future studies should use these systems more to explore the convergent/divergent evolution of sex chromosomes. 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

“…The nonrandom co-option of certain genomic regions could reflect a limited pool of genes involved in gonadal development ('usual suspects' such as amh, ar, dmrt1 or sox3) that can evolve as a master sex-determining gene by turning their syntenic blocks into sex chromosomes. Indeed, certain syntenic blocks seem to emerge more often as sex chromosomes in ranid frogs [71] and amniotes, but at least in amniotes, this non-random pattern is not particularly strong [34]. The numerous exceptions can be caused by the emergence of a sex-determining locus via duplication within a different syntenic block from the original one with the 'usual suspect' gene, or by the existence of more genes with a potential to become sex-determining genes than we assume.…”

“…And vice versa, that two taxa exhibit the same chromosome pair as sex chromosomes does not necessarily mean their sex determination systems are homologous: the same pair of autosomes can be independently co-opted for the function of sex chromosomes (e.g. [71,75,128]; for overview in amniotes see [34]), or there might be turnovers of sex determination systems by the emergence of a new sex-determining locus within the same sex chromosome pair [66,129] (cases 15, 18 and 20 in figure 2).…”

“…the lineage including reptiles and birds), such as turtles [12,31,32], which points to non-homology of sex chromosomes across amniote GSD lineages (but see e.g. [33], critically discussed in [34]). Recently, Straková et al [35] suggested that ESD in amniotes evolved from ancestral sequential hermaphroditism, which turned into ESD via a heterochronic shift, that is, by moving the timing of the ontogenetic period of sex change from the adult to the embryo.…”

A brief review of vertebrate sex evolution with a pledge for integrative research: towards ‘sexomics’

“…Highly diverse sex chromosomes may derive from frequent turnovers of SD genes [12,13], suggesting that new SD systems may evolve de novo and independently. Deep homology of some sex chromosome systems across disparate taxa suggest that gene content may predispose certain linkage groups to become sex chromosomes [4,[14][15][16], however, so far with relatively weak support in amniotes [17]. Numerous theoretical concepts and models about transitions among SD systems, degeneration and turnover of sex chromosomes [18][19][20][21][22][23] often remain to be empirically tested in vertebrates.…”

Preface

“…-Co-option of the same linkage groups into sex chromosomes [15,16]; -Is differentiation of sex chromosomes a unidirectional pathway? [17,18]; -Consequences of differentiated sex chromosomes [19]; -Differences in differentiation of sex chromosomes under male versus female heterogamety [20,21]; -Evolution of sex chromosomes under hybridization and polyploidy [23][24].…”