The human Y chromosome began to evolve from an autosome hundreds of millions of years ago, acquiring a sex-determining function and undergoing a series of inversions that suppressed crossing over with the X chromosome1, 2. Little is known about the recent evolution of the Y chromosome because only the human Y chromosome has been fully sequenced. Prevailing theories hold that Y chromosomes evolve by gene loss, the pace of which slows over time, eventually leading to a paucity of genes, and stasis3, 4. These theories have been buttressed by partial sequence data from newly emergent plant and animal Y chromosomes5, 6, 7, 8, but they have not been tested in older, highly evolved Y chromosomes such as that of humans.
Here we finished sequencing of the male-specific region of the Y chromosome (MSY) in our closest living relative, the chimpanzee, achieving levels of accuracy and completion previously reached for the human MSY. By comparing the MSYs of the two species we show that they differ radically in sequence structure and gene content, indicating rapid evolution during the past 6 million years. The chimpanzee MSY contains twice as many massive palindromes as the human MSY, yet it has lost large fractions of the MSY protein-coding genes and gene families present in the last common ancestor.
We suggest that the extraordinary divergence of the chimpanzee and human MSYs was driven by four synergistic factors: the prominent role of the MSY in sperm production, ‘genetic hitchhiking’ effects in the absence of meiotic crossing over, frequent ectopic recombination within the MSY, and species differences in mating behaviour. Although genetic decay may be the principal dynamic in the evolution of newly emergent Y chromosomes, wholesale renovation is the paramount theme in the continuing evolution of chimpanzee, human and perhaps other older MSYs.
The rest of the content is behind Nature’s paywall, but Hawks offers some additional comment regarding the rest of the paper, specifically three options that might account for the unexpected gulf of difference, described within the paper thus:
Indeed, at 6 million years of separation, the difference in MSY gene content in chimpanzee and human is more comparable to the difference in autosomal gene content in chicken and human, at 310 million years of separation.
Option 1: Maybe nothing, Option 2: Massive changes in gene regulation, and Option 3: Hitchhiking, all of which is which is prefaced by this:
The Y chromosome was part of the initial chimpanzee genome draft, and was recognized then as a “clear outlier” in showing low human-chimpanzee sequence similarity (Chimpanzee Genome Consortium 2005). But it wasn’t obvious just how different it was because the relatively short sequencing reads aligned fairly well with the human draft. That comparison also seems not to have included the missing genes (they might have just been missed during sequencing), or duplications. Moreover, the Y chromosome includes a high fraction of repetitive sequence, including long front-to-back, or “palindromic” passages.
Only with very long reads with long overlaps is it possible to straighten out the large-scale sequence, and thereby detect sequence reorganizations and large copy number variants. This kind of intensive sequencing has so far been completed only for chromosome 21 and now the Y chromosome.
To read the rest of his commentary, just head over to Hawks’ Weblog.
Hughes JF and 16 others. 2010. Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature (early online) doi:10.1038/nature08700