Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes

Abstract

In therian mammals (placentals and marsupials), sex is determined by an XX female: XY male system, in which a gene (SRY) on the Y affects male determination. There is no equivalent in other amniotes, although some taxa (notably birds and snakes) have differentiated sex chromosomes. Birds have a ZW female: ZZ male system with no homology with mammal sex chromosomes, in which dosage of a Z-borne gene (possibly DMRT1) affects male determination. As the most basal mammal group, the egg-laying monotremes are ideal for determining how the therian XY system evolved. The platypus has an extraordinary sex chromosome complex, in which five X and five Y chromosomes pair in a translocation chain of alternating X and Y chromosomes. We used physical mapping to identify genes on the pairing regions between adjacent X and Y chromosomes. Most significantly, comparative mapping shows that, contrary to earlier reports, there is no homology between the platypus and therian X chromosomes. Orthologs of genes in the conserved region of the human X (including SOX3, the gene from which SRY evolved) all map to platypus chromosome 6, which therefore represents the ancestral autosome from which the therian X and Y pair derived. Rather, the platypus X chromosomes have substantial homology with the bird Z chromosome (including DMRT1) and to segments syntenic with this region in the human genome. Thus, platypus sex chromosomes have strong homology with bird, but not to therian sex chromosomes, implying that the therian X and Y chromosomes (and the SRY gene) evolved from an autosomal pair after the divergence of monotremes only 166 million years ago. Therefore, the therian X and Y are more than 145 million years younger than previously thought.

Did sex chromosome turnover promote divergence of the major mammal groups?

“…Mapping the genes on the five X and five Y chromosomes confirmed that platypus sex chromosomes have no homology to the therian X. But, surprisingly, they have extensive homology to the bird ZW sex chromosome pair 52.…”

“…Sequence comparisons between X‐Y shared genes revealed that the large X 5 and tiny Y 5 that terminate the chain are the most diverged, and therefore the oldest members of the chain 54, suggesting that they represent the original mammalian sex chromosomes. X 5 is largely homologous to the bird Z 52.…”

The origin and evolution of vertebrate sex chromosomes and dosage compensation

“…Surprisingly, it was found that none of the platypus X chromosomes share homology with the therian X chromosome (Veyrunes et al, 2008). Instead, the conserved region of the therian X chromosome is homologous to platypus chromosome 6 (Veyrunes et al, 2008), whereas the added region of the eutherian sex chromosomes is orthologous to parts of chromosomes 15q and 18p (Veyrunes et al, 2008) (Figure 2). The observation that therian X chromosome is represented by an autosome in monotremes unambiguously dates the origin of the therian sex chromsomes to after the divergence of monotermes from therians (166 MYA), but before the therian radiation (148 MYA).…”

The role of repetitive DNA in structure and evolution of sex chromosomes in plants

“…In general, regions with suppressed or no recombination tend to accumulate repetitive DNA sequences (for review see Charlesworth et al, 1994;Gvozdev et al, 2005). Nonrecombining parts of the Y chromosome have accumulated repetitive DNA, particularly in the mammalian (Erlandsson et al, 2000;Skaletsky et al, 2003) and Drosophila melanogaster (Pimpinelli et al, 1995) Y chromosomes, which are evolutionarily ancient, originating before 165 and 60 mya, respectively (Graves, 2005;Veyrunes et al, 2008). However, the process of accumulation of repetitive sequences is apparent even in evolutionarily young sex chromosomes, such as in Drosophila miranda (Steinemann and Steinemann, 1992), Silene latifolia (Hobza et al, 2006;Kejnovsky et al, 2006a) or Carica papaya (Liu et al, 2004).…”