I HAD PLANNED on covering the article on the platypus genome that came out in Nature last week, but since then this paper has been discussed in detail on Pharyngula and Adaptive Complexity and I think further discussion would be moot. I did notice while reading the paper that the unfortunate description of certain platypus genes as “reptilian” cropped up frequently. Although the authors noted that the sauropsids and synapsids are amniotes, they never mentioned that platypus genes shared with reptiles are actually basal amniote genes. Although their phylogenetic tree shows synapsids and sauropsids clearly diverging from a common amniote ancestor, they do not seem to realize referring to these ancestral amniote genes as “reptilian” suggests evolution of the platypus (and thus all synapsids) from reptiles instead of from a non-reptilian amniote.

However, today I want to talk about the platypus’ sex chromosomes. Platypuses, like the therians, have genetic sex determination. They have an XX/XY system in which males (XY) are the heterogametic sex. Many reptiles have environmental sex determination, with sex determined by factors such as incubation temperature during embryonic development. However, some reptiles and all birds have a ZW/ZZ sex determination system, with females (ZW) as the heterogametic sex.

Something as basic as sex determination seems necessarily static and unchanging, but in actuality sex chromosomes and sex determination systems evolve, sometimes very rapidly. I mentioned in a previous post the gradual tightening of Muller’s ratchet, which in the absence of translocation of new DNA from another chromosome will eventually destroy the Y chromosome (or the W chromosome in ZW heterogametic organisms). There too I mentioned the way that some mole voles have already lost the Y chromosome, with sex determination now based upon a gene on some autosomal chromosome, which will now be under selection for the accumulation of male-benefiting genes and may evolve into a new set of sex chromosomes. Karyotype studies of the platypus shows a different but equally strange phenomenon—ten sex chromosomes.1 While this oddity was obvious early on, the new paper from Genome Research firmly establishes a different phenomenon, which was anticipated by some researchers. While monotremes and therians both have XY/XX systems, the monotreme X and Y chromosomes evolved independently, and the monotreme X chromosomes have significant sequence similarities to the avian Z chromosome.2

This is consistent with basal amniotes possessing early prototypes of the avian W and Z chromosomes. These were passed on to the sauropsid and synapsid lines. Among the sauropsids, some evolved other methods for sex determination while others retained the W and Z chromosomes, or in the case of the snakes evolved their own versions of the W and Z chromosomes. On the synapsid line it is hard to say what other sex determination systems may have evolved, since there are only a few closely-related extant lineages of synapsids. Veyrunes, Waters, and coworkers found that the presence of sex chromosomes with sequence similarity to avian Z chromosomes in monotremes shows that the line leading to mammals kept the amniote proto-ZW/ZZ system for quite a while. After the monotreme/therian divergence the monotremes began evolving from a ZW/ZZ system to a XY/XX system. Since there are only two extant monotremes, the platypus and the echidna, it is hard to say when the monotreme’s multiple sex chromosomes evolved. The platypus has ten sex chromosomes, while the echnidna has nine (five X’s and four Y’s).3 The monotremes manage to keep these multiple chromosomes coordinated by homology between the ends of the chromosomes, so they line up in a chromosomal chain.

Phylogenetic tree of sex chromosomesAlong the line to marsupials and placental mammals our ancestors lost their dependence upon the ZW/ZZ system and evolved the therian X and Y chromosomes. Veyrunes and Waters report that genes on our X chromosome map to orthologs found on platypus chromosome 6, an autosomal chromosome. The ancestor of this chromosome 6 probably evolved into our X chromosome on the line to the modern therians. Since the marsupial and placental mammal sex chromosomes are homologous, the therian XY/XX system evolved by the time the marsupials and placental mammals diverged, although these chromosomes have undergone subsequent changes in both lineages. Meanwhile the ancestral W and Z sex chromosomes over time fragmented by translocations to other chromosomes and losses to deletions. The remnants of the ancestral Z chromosome are scattered over several autosomal chromosomes. Some of the details of these transformations can be seen in the phylogenetic tree from Genome Research shown to the right.2

Importantly, monotremes lack SRY (sex-determining Y), a gene critical in male gonadogenesis in therians. SRY evolved from the SOX3 gene, which likewise maps to platypus chromosome 6. I speculate that the trigger for the evolution of our XY/XX system is the evolution of SRY. As this gene began to take a role in male sexual differentiation selection would favor the limitation of recombination between the proto-Y chromosome and the proto-X chromosome and the segregation of male-specific genes on the new Y chromosome.4 However, it is also possible that SRY took over from some other gene that kicked off the differentiation of this previously autosomal chromosome pair into two new sex chromosomes.4

While the presentation of this discovery has not been as misleading as the Nature article on the full genome, there are some problems that T. Ryan Gregory points out at Genomicron. As I mentioned before, we should not expect a trait possessed by monotremes to be primitive simply based upon the monotremes’ divergence some 20 million years before the divergence of marsupials and placental mammals. When the monotremes diverged from the therians both lineages possessed an equal number of ancestral traits, and both lineages have evolved since then. Indeed, the information in this paper shows that the picture is more complicated than a simple summary of monotremes as “basal”. While the monotreme and therian lineages both inherited the ancestral W and Z chromosomes, both lineages then evolved their own X and Y chromosomes to replace these. The monotreme XY/XX system is as innovative as the therian XY/XX system.

  1. Rens, W.; Grützner, F.; O’Brien, P. C. M.; Fairclough, H.; Graves, J. A. M.; Ferguson-Smith, M. A. “Resolution and evolution of the duck-billed platypus karyotype with an X1Y1X2Y2X3Y3X4Y4X5Y5 male sex chromosome constitution.” Proceedings of the National Academy of Sciences 2004, 101, 16257-16261. doi:10.1073/pnas.0405702101
  2. Veyrunes, F.; Waters, P. D.; Miethke, P.; Rens, W.; McMillan, D.; Alsop, A. E.; Grützner, F.; Deakin, J. E.; Whittington, C. M.; Schatzkamer, K.; Kremitzki, C. L.; Graves, T.; Ferguson-Smith, M. A.; Warren, W.; Graves, J. A. M. “Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes.” Genome Research, published online before print May 7, 2008 doi:10.1101/gr.7101908
  3. Rens, W.; O’Brien, P. C. M.; Grützner, F.; Clarke, O.; Graphodatskaya, D.; Tsend-Ayush, E.; Trifonov, V. A.; Skelton, H.; Wallis, M. C.; Johnston, S.; Veyrunes, F.; Graves, J. A. M.; Ferguson-Smith, M. A. “The multiple sex chromosomes of platypus and echidna are not completely identical and several share homology with the avian Z.” Genome Biology 2007, 8, R243. doi:10.1186/gb-2007-8-11-r243
  4. Waters, P. D.; Wallis, M. C.; Graves, J. A. M. “Mammalian sex—Origin and evolution of the Y chromosome and SRY.” Seminars in Cell & Developmental Biology 2007, 18, 389-400. doi:10.1016/j.semcdb.2007.02.007