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The inevitability of sex chromosome degeneration

tonguefish_brenda-bridgettI’m as cynical as anyone about Yet-Another-Genome Syndrome (though it seems to have leveled off in the past few years as sequencing as become accessible enough that people really want to focus on biology earlier on). But a new paper in Nature Genetics, Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle, shows the value of the approach when you’re actually looking at an interesting topic. Though most people might not be fascinated by the flatfish, many are curious about the nature of sex determination. You are likely familiar with the standard XY system of placental mammals, but non-placentals, birds, insects, etc. have different frameworks (and though Drosophila is also XY, it’s not quite the same as the mammalian system).

Though  I suspect our big-picture understanding of the origin and diversification of sex chromosomes is going to be enabled far more by the work on Drosophila, the authors make some good arguments for why this organism might give us insights. With a small genome, presumably it was technically easier to assemble. Additionally, teleost fish have young sex chromosomes, so whatever general forces reshape this region of the genome is going to be incipient. Like birds, the flatfish have a ZW sex-determination system. This means that females, not males, are the heterogametic sex. So in flatfish, like birds, females would express sex-linked diseases. Or at least that’s the expectation.

It turns out that the 30 million year old W chromosome hasn’t lost nearly as many of the functional gene copies as the bird W (or the mammal Y). There has been some gene loss, but it isn’t nearly as degenerated as the chromosomes of lineages where the system of sex-determination has an older origin. The authors claim that the mammalian system for example is hundreds of millions of years old. This puts into stark relief how ludicrous it was when Bryan Sykes began to assert that the mammalian Y chromosome was on its last legs, and that mammals were well nigh on the verge of going extinct (due to the disappearance of males). These results show that sex chromosomes can persist in a gene-poor state for a very long while. Though gene loss isn’t nearly as total on the bird W or mammalian Y, it has been significant even in these flatfish, indicating that much of the degeneration occurred early on in many lineages.

The reason that understanding of the evolution of sex-determination is important is that the phenomenon illustrates the constraints imposed by the nature of our genomic architecture. The rise and fall and rise of sex chromosomes can perhaps tell us about the borders of the canvas upon with evolution must work. Evolutionary genetic change is not just about possibilities, but also the rules of the game.

Citation: Nature Genetics (2014) doi:10.1038/ng.2890

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