Low conservation of gene content in the Drosophila Y chromosome

Abstract

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). 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), and the same linkage groups are clearly recognizable in mosquito genomes (260 Myr of divergence). 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 chromosomes, 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.

Figure 1. Synteny analysis of the kl-5 gene

The gene is Y-linked in all examined Drosophila species except D. willistoni (and in D. pseudoobscura / D. persimilis), which might suggest a Y-to-autosome transfer in the D. willistoni lineage. However, the conserved synteny between D. willistoni and Anopheles gambiae (panel A) shows that the autosomal D. willistoni location is ancestral (thick lines in panel B). Hence, there were two independent transfers of kl-5 to the Y chromosome (arrows in panel B). Note that the Drosophila CG3330 gene has no ortholog in Anopheles. See Supplementary Fig. 4 for the remaining species.

Figure 2. Gene movements in the Drosophila Y

Gene gains (red arrows) and losses (blue arrows) were inferred by synteny. For changes that occurred before the split of the Drosophila and Sophophora subgenera (genes kl-2, kl-3, ORY, PRY, PPr-Y; dashed arrows) there is no close outgroup for inferring the direction (gain vs. loss) through synteny. However, all five genes are autosomal or X-linked in Anopheles, which suggests that they were acquired by the Y chromosome between 260 Myr (i.e., the Drosophila - Anopheles divergence time3,5 ) and 63 Myr ago.

Figure 3. Posterior density of net rate of Y-linked gene gain in the Drosophila phylogeny

A Bayesian rejection sampling procedure was applied (see text) to yield 1,000 estimates of rates of gene gain and loss conditional on the observed gains and losses of genes on the Y chromosome, and conditional on the genes being observed in D. melanogaster (matching the actual ascertainment of Y genes used in this study). The average of net gain rate (gain rate minus loss rate) is + 0.130 genes / Myr, and all 1,000 simulations had a higher rate of gene gain than loss (range of net gain rate: + 0.035 to + 0.352).