Non-homologous sex chromosomes of birds and snakes share repetitive sequences

Abstract

Snake sex chromosomes provided Susumo Ohno with the material on which he based his theory of how sex chromosomes differentiate from autosomal pairs. Like birds, snakes have a ZZ male/ZW female sex chromosome system, in which the snake Z is a macrochromosome much the same size as the bird Z. However, the gene content shows clearly that the snake and bird Z chromosomes are completely non-homologous. The molecular aspect of W chromosome degeneration in snakes remains largely unexplored. We used comparative genomic hybridization to identify the female-specific region of the W chromosome in representative species of Australian snakes. Using this approach, we show that an increasingly complex suite of repeats accompanies the evolution of W chromosome heteromorphy. In particular, we found that while the python Liasis fuscus exhibits no sex-specific repeats and indeed, no cytologically recognizable sex-specific region, the colubrid Stegonotus cucullatus shows a large domain on the short arm of the W chromosome that consists of female-specific repeats, and the large W of Notechis scutatus is composed almost entirely of repetitive sequences, including Bkm and 18S rDNA-related elements. FISH mapping of both simple and complex probes shows patterns of repeat amplification concordant with the size of the female-specific region in each species examined. Mapping of intronic sequences of genes that are sex-linked in both birds (DMRT1) and snakes (CTNNB1) reveals massive amplification in discrete domains on the W chromosome of the elapid N. scutatus. Using chicken W chromosome paint, we demonstrate that repetitive sequences are shared between the sex chromosomes of birds and derived snakes. This could be explained by ancestral but as yet undetected shared synteny of bird and snake sex chromosomes or may indicate functional homology of the repeats and suggests that degeneration is a convergent property of sex chromosome evolution. We also establish that synteny of snake Z-linked genes has been conserved for at least 166 million years and that the snake Z consists of two conserved blocks derived from the same ancestral vertebrate chromosome.

Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae)

“…Noteworthy, it was evidenced that the end of the Wq has a high concentration of female-specific sequences (Figures 2-4), where an 18S rDNA cluster is also located in all Triportheus species so far analyzed (Artoni and Evolution of sex chromosomes in congeneric species CF Yano et al Bertollo, 2002;Nirchio et al, 2007;Diniz et al, 2009;Marquioni et al, 2013;Yano et al, 2014). Sex chromosomes carrying 18S rDNA sequences have already been reported in several other vertebrates, such as Characidium fishes (Scacchetti et al, 2015), cane toad Bufo marinus (Abramyan et al, 2009), Chinese softshell turtle Pelodiscus sinensis (Kawai et al, 2007) and tiger snake Notechis scutatus (O'Meally et al, 2010). However, the Triportheus case deserves further considerations because of the unusual and particular location of these sequences that do not occur in both homologs of the sex pair (only on the W chromosome) and in some autosomes.…”

Molecular cloning and characterization of the repetitive DNA sequences that comprise the constitutive heterochromatin of the W chromosomes of medaka fishes

“…Sex chromosomes bearing rDNAs/NORs have been reported in some vertebrates, such as mammals, reptiles, and amphibians (Kawai et al 2007;O'Meally et al 2010;Schmid et al 1983;Wiley 2003), suggesting that the accumulation of rDNAs is a common property of sex chromosome differentiation in vertebrates. Strong signals of rDNAs/NORs were observed on X or W chromosome in these cases; therefore, the copy number of the rRNA genes was considered to be higher in females than in males, implying a functional significance for female-specific amplification of NORs.…”

Are some chromosomes particularly good at sex? Insights from amniotes

“…The snake Z bears orthologs of genes on chicken chromosomes 2p and 27. To date, 29 genes mapped to the snake Z have orthologs on these two chicken chromosomes (K. Matsubara, personal communication), indicating that this chromosome arose by fusion of ancestral segments represented by chicken chromosomes 2p and 27 after a translocation between Z and 2 in sauropsid ancestor (O'Meally et al 2010). Synteny of chicken 2 and Z genes is conserved in monotremes (Rens et al 2007), suggesting that the translocation occurred in an amniote ancestor.…”