Low conservation of gene content in the Drosophila Y chromosome

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Abstract
Chromosomal organization is by and large evolutionarily stable. In Drosophila over 95% of the genes have remained on the same chromosome arm in 12 species that diverged about 63 million years ago. A study of Y chromosomes, however, reveals that only a quarter of D. melanogaster Y-linked genes are also Y-linked in the other 11 sequenced species. And in contrast to the mammalian Y chromosome, a picture of degeneration and gene loss, gene gains on the Drosophila Y chromosome outnumber losses by more than ten to one. In Drosophila more than 95% of the genes have remained on the same chromosome arm in 12 species that diverged 63 Myr ago. This study finds that only a quarter of D. melanogaster Y linked genes are also Y-linked in these 12 species. Gene losses are known to play a major role in the evolution of Y chromosomes, but this study shows that in contrast with the mammalian Y, gene gains play an important role in the evolution of the Drosophila Y chromosome. Chromosomal organization is sufficiently evolutionarily stable that large syntenic blocks of genes can be recognized even between species as distantly related as mammals and puffer fish (450 million years (Myr) of divergence)1,2,3,4,5,6,7. In Diptera, the gene content of the X chromosome and the autosomes is well conserved: in Drosophila more than 95% of the genes have remained on the same chromosome arm in the 12 sequenced species (63 Myr of divergence, traversing 400 Myr of evolution)2,4,6, and the same linkage groups are clearly recognizable in mosquito genomes (260 Myr of divergence)3,5,7. Here we investigate the conservation of Y-linked gene content among the 12 sequenced Drosophila species. We found that only a quarter of the Drosophila melanogaster Y-linked genes (3 out of 12) are Y-linked in all sequenced species, and that most of them (7 out of 12) were acquired less than 63 Myr ago. Hence, whereas the organization of other Drosophila chromosomes traces back to the common ancestor with mosquitoes, the gene content of the D. melanogaster Y chromosome is much younger. Gene losses are known to have an important role in the evolution of Y chromosomes8,9,10, and we indeed found two such cases. However, the rate of gene gain in the Drosophila Y chromosomes investigated is 10.9 times higher than the rate of gene loss (95% confidence interval: 2.3–52.5), indicating a clear tendency of the Y chromosomes to increase in gene content. In contrast with the mammalian Y chromosome, gene gains have a prominent role in the evolution of the Drosophila Y chromosome.