Comparative genomics reveals a constant rate of origination and convergent acquisition of functional retrogenes in Drosophila

Abstract

Background: Processed copies of genes (retrogenes) are duplicate genes that originated through the reverse-transcription of a host transcript and insertion in the genome. This type of gene duplication, as any other, could be a source of new genes and functions. Using whole genome sequence data for 12 Drosophila species, we dated the origin of 94 retroposition events that gave rise to candidate functional genes in D. melanogaster.

Results: Based on this analysis, we infer that functional retrogenes have emerged at a fairly constant rate of 0.5 genes per million years per lineage over the last approximately 63 million years of Drosophila evolution. The number of functional retrogenes and the rate at which they are recruited in the D. melanogaster lineage are of the same order of magnitude as those estimated in the human lineage, despite the higher deletion bias in the Drosophila genome. However, unlike primates, the rate of retroposition in Drosophila seems to be fairly constant and no burst of retroposition can be inferred from our analyses. In addition, our data also support an important role for retrogenes as a source of lineage-specific male functions, in agreement with previous hypotheses. Finally, we identified three cases of functional retrogenes in D. melanogaster that have been independently retroposed and recruited in parallel as new genes in other Drosophila lineages.

Conclusion: Together, these results indicate that retroposition is a persistent mechanism and a recurrent pathway for the emergence of new genes in Drosophila.

Figure 1

Retrogene phylogenetic distribution with respect to the analyzed sequenced genomes. Divergence times in each node are indicated. Branches are numbered below and the number of retroposition events in the particular internal branches is shown on top of the branch. The estimated rate of retroposition is shown in every internal node.

Figure 2

Drosophila phylogeny showing a summary of our inferences about the time of the independent parallel retroposition events from the parental genes Cervantes, Dntf-2 and Ran. Note that some of these events (for Dntf-2 and Ran) overlap, as discussed in the text.