Origin of Amniote Sex Chromosomes: An Ancestral Super-Sex Chromosome, or Common Requirements?

Abstract

The diversity of sex chromosomes among amniotes is the product of independent evolution of different systems in different lineages, defined by novel sex-determining genes. Convergent evolution is very common, suggesting that some genes are particularly adept at taking on a sex-determining role. Comparative gene mapping, and more recently whole genome sequencing, have now turned up other surprising relationships; different regions of the amniote genome that have become sex determining in some taxa seem to share synteny, or share sequence, in others. Is this, after all, evidence that these regions were once linked in a super-sex chromosome that underwent multiple fission in different ways in different amniote lineages? Or does it signify that special properties of sex chromosomes (paucity of active genes, low recombination, epigenetic regulation to achieve dosage compensation) predispose particular chromosomes to a sex-determining role?

ZZ/ZW Sex Chromosomes in the Endemic Puerto Rican Leaf-Toed Gecko (<b><i>Phyllodactylus wirshingi</i></b>)

“…Furthermore, comparative FISH analyses using fluorescently labeled chromosome paints have shown that the sex chromosomes of additional geckos, Lialis burtonis (XXXX/ XXY), Coleonyx elegans (XXXX/XXY), and C. marmoratus (ZZ/ZW), are not homologous to the avian ZZ/ZW [Pokorná et al, 2011;Matsubara et al, 2014]. Because P. wirshingi and G. hokouensis possess ZZ/ZW sex chromosomes that are homologous with the avian Z, it is worth asking whether their ZZ/ZW sex chromosomes are derived from a common ancestor with "avian ZW" sex chromosomes [Ezaz et al, 2017]. While not impossible, it appears unlikely in this case.…”

“…There are several competing hypotheses to address this. For example, it has been hypothesized that one or more of these extant sex chromosome systems are ancestral and thus exist in multiple lineages due to inheritance from a common ancestor [Graves and Peichel, 2010;O'Meally et al, 2012;Ezaz et al, 2017]. As mentioned above, this seems unlikely, at least in geckos.…”

Understanding the Evolution of Reptile Chromosomes through Applications of Combined Cytogenetics and Genomics Approaches

“…Although there have been a number of in silico studies to infer sex chromosome homologies of reptiles, in particular with chicken [e.g., for review see Ezaz et al, 2017], physical mapping of sex chromosome genes have only been reported for 3 species of snakes, 4 species of turtles, and 4 species of lizards [Matsubara et al, 2006;Kawagoshi et al, 2009Kawagoshi et al, , 2012Kawagoshi et al, , 2014Kawai et al, 2009;Alföldi et al, 2011;Ezaz et al, 2013;Srikulnath et al, 2014;Deakin et al, 2016;Montiel et al, 2017]. In these studies, sex chromosome-specific cDNA or BAC clones were isolated by a candidate gene approach and physically mapped to validate their sex chromosomal origin, and their homology to chicken chromosomes was inferred.…”

“…These studies have identified homologies of reptile XY and ZW sex chromosomes with 9 different chicken chromosomes (2,5,6,9,15,17,23,27, and ZW) including 2 species of reptiles -a lizard ZW ( G. hokouensis ) and turtle XY ( S. triporcatus and S. salvinii ) -sharing homology with chicken ZW chromosomes ( Fig. 4 ) [reviewed in Montiel et al, 2016;Ezaz et al, 2017]. This suggests multiple origins of reptilian sex chromosomes from multiple ancestral proto-sex chromosomes ( Fig.…”

“…Some species have significantly differentiated sex chromosomes, allowing them to be easily identified using standard karyotyping, but other species have cryptic sex chromosomes, requiring more sophisticated approaches for them to be discovered [Ezaz et al, 2005;Martinez et al, 2008]. By comparing reptile genomes, we are able to trace the origin of sex chromosomes and gain general insight in sex chromosome evolution [Ezaz et al, 2017].…”