A few months ago I wrote the following:
I should point out that the mammalian Y chromosome is an anomaly in origin and sex determination. In fact, every single sex determination system and sex chromosome system that I know of differs from all of the others in some manner. It looks like I'm going to have to write an entry on the evolutionary genetics of sex determination in everything other than mammals.
I never did get around to writing that review of sex chromosomes. All is not lost, however, as the most recent issue of Current Biology is devoted to the evolution of sex. There is even an article that reviews sex chromosome evolution in vertebrates. It is from that article that I take this week's phylogeny:
Figure 1. Vertebrate sex determination systems.
Phylogeny of major vertebrate clades showing the sex determining systems found in members of the respective clade. 'Mulitple' indicates involvement of more than one pair of chromosomes in sex determination. Dates of divergence are taken from 42, 82 and 83. TSD: temperature-dependent sex determination.
The XX/XY system is the one with which most people are familiar -- males are heterogametic (XY), and females are homogametic (XX). The Y chromosome confers the male phenotype in humans, for example. Monotremes (ie, platypus) have multiple sex chromosomes that form a chain (reviewed here). In other taxa (birds, some other reptiles, some fish, and lepidopterans) males are homogametic (ZZ) and females are heterogametic (ZW). Additionally, many taxa use developmental environment to determine sex, and others can change sex during their life based on environmental cues.
While sexual reproduction is the ancestral state amongst vertebrates (and probably amongst all animals), sex determination systems have evolved multiple times. It is thought that the bird Z and W chromosomes evolved independently from the mammalian X and Y, but data from the platypus genome suggest otherwise. The chain of sex chromosomes in platypus contains the homolog of the avian Z and W on one end and the homolog of the mammalian X and Y at the other. Furthermore, the gene content of the X and Z chromosomes indicates similar selection against potentially deleterious mutations on these two chromosomes. This leads some people to believe that the ancestor of reptiles and mammals had a sex chromosome karyotype like that of monotremes, and one pair of sex chromosomes were retained along the mammalian lineage and a different pair along the lineage leading to birds.
The avian and mammalian W and Y chromosomes are the result of the degradation of the Z and X chromosomes, respectively. An ancestral autosomal pair became specialized as a sex chromosome, with one homolog degrading into the chromosome found in the heterogametic sex. Another well studied system, Drosophila, reveals a different story of sex chromosome evolution. In the case of Drosophila, Y chromosomes are not homologous across the entire taxa. Instead, new Y chromosomes evolve when autosomes fuse with X or Y chromosomes. When this occurs, the homolog of the fused autosome degrades into a new Y chromosome. For an example of such a fusion-degradation event, see here.
T Ezaz, R Stiglec, F Veyrunes, and JAM Graves. 2006. Relationships between Vertebrate ZW and XY Sex Chromosome Systems. Current Biology 16: R736-R743. doi:10.1016/j.cub.2006.08.021
AB Carvalho and AG Clark. 2005. Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307: 108-110. doi:10.1126/science.1101675
Great post...thanks for pointing this phylogeny out...very timely since this is what I was just covering in my lecture, though not as completely.
Last spring I read the platypus paper in some detail for a seminar I was leading.
The evidence for multiple X and multiple Y chromosomes with a complicated pairing arrangement seems strong. I was not convinced by the argument that this is a link between placental XY systems and avian ZW systems. The evidence, if I remember correctly, is that the chromosome at one end of the chain contains a DMRT1 type gene (implicated in masculinization and mapping on the avian Z) and the chromosome at the other end contains a SOX3 like gene (SOX3 being a putative ancestor to SRY of placentals).
The stratiography of human and chimp X and Y chromosomes, as well as comparison to chicken chromosomes, seems to track the X to two different, not overly rearranged avian autosomes, and further defines a pathway that looks very much like the previously hypothesized series of progressive steps of recombination suppression and degeneration. At least on the face of it, this does not look like a variant of a system in place with the common ancestor of birds, echidnas, platypuses and placentals.
Mike, the Current Biology review also points to the content of cancer related genes in eutherian and avian X chromosomes and autosomes. Both the human X and chicken Z are depleted for cancer related genes (relative to the autosomes). This may be because the X is hemizygous in the heterogametic sex.
Interestingly, the regions of the human genome homologous to the chicken Z also show a depletion of cancer related genes. The authors argue that this inidicates an ancestral sex chromosome state for those regions. It's not that the X and Z are homologous, but that they used to be joined in a chain of sex chromosomes.