ORIGINAL ARTICLE
doi:10.1111/evo.12151
HOMOLOGOUS SEX CHROMOSOMES IN THREE DEEPLY DIVERGENT ANURAN SPECIES
Alan Brelsford,1,2 Matthias Stock,¨ 1,3 Caroline Betto-Colliard,1 Sylvain Dubey,1 Christophe Dufresnes,1 Hel´ ene` Jourdan-Pineau,1 Nicolas Rodrigues,1 Romain Savary,1 Roberto Sermier,1 and Nicolas Perrin1 1Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland 2E-mail: [email protected] 3Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Muggelseedamm¨ 310, D-12587, Berlin, Germany
Received February 6, 2013 Accepted April 15, 2013 Data Archived: Dryad doi:10.5061/dryad.5nt3g; GenBank KF017619-KF017623, KF053415-KF053429; NCBI SRA SRP021099
Comparative genomic studies are revealing that, in sharp contrast with the strong stability found in birds and mammals, sex determination mechanisms are surprisingly labile in cold-blooded vertebrates, with frequent transitions between different pairs of sex chromosomes. It was recently suggested that, in context of this high turnover, some chromosome pairs might be more likely than others to be co-opted as sex chromosomes. Empirical support, however, is still very limited. Here we show that sex-linked markers from three highly divergent groups of anurans map to Xenopus tropicalis scaffold 1, a large part of which is homologous to the avian sex chromosome. Accordingly, the bird sex determination gene DMRT1, known to play a key role in sex differentiation across many animal lineages, is sex linked in all three groups. Our data provide strong support for the idea that some chromosome pairs are more likely than others to be co-opted as sex chromosomes because they harbor key genes from the sex determination pathway.
KEY WORDS: Amphibian, Bufo siculus, convergent evolution, conserved synteny, DMRT1, Hyla arborea, Rana temporaria,sex chromosome turnover..
Sex chromosomes have been a focus of evolutionary biology for Two recent reviews have suggested that some chromosomes a long time, but until recently, most research has focused on might be more likely than others to carry the master sex de- organisms with well-differentiated sex chromosomes, such as fruit termination gene, through conservation of an ancestral system flies, mammals, and birds (Bachtrog et al. 2011). In contrast, sex of sex determination or the reuse of a small set of genes that chromosomes are much less differentiated in most amphibians, can capture the top position in the pathway (Graves and Peichel reptiles, and fishes. Cold-blooded vertebrates also differ from 2010, O’Meally et al. 2012). Thus far, few empirical examples are mammals and birds in displaying a relatively high rate of transition available to support this hypothesis: among amniotes, the same in sex determination systems. The sex-determining locus is often chromosome is sex linked in birds, monotremes, and one lizard found on nonhomologous chromosomes in closely related species, species, and another chromosome is sex linked in both a turtle or even within single species (Charlesworth and Mank 2010). and a lizard species (O’Meally et al. 2012). However, neither the This diversity is at first surprising, given the strong conservation snake nor the therian sex chromosomes are known to be sex linked of elements of the sex determination pathway across animals in any other amniote (O’Meally et al. 2012). In fish, eight differ- (Raymond et al. 1998), but may be explained by mutations causing ent chromosomes are sex linked among the 16 cases reviewed different genes to take over the top position in a conserved sex by Graves and Peichel (2010). In insects, no homology is evi- determining cascade (Wilkins 1995; Schartl 2004; Volff et al. dent between the sex chromosomes of Diptera, Lepidoptera, and 2007; Graves 2013). Coleoptera (Pease and Hahn 2012).