On the origin of new genes in Drosophila

Abstract

Several mechanisms have been proposed to account for the origination of new genes. Despite extensive case studies, the general principles governing this fundamental process are still unclear at the whole-genome level. Here, we unveil genome-wide patterns for the mutational mechanisms leading to new genes and their subsequent lineage-specific evolution at different time nodes in the Drosophila melanogaster species subgroup. We find that (1) tandem gene duplication has generated approximately 80% of the nascent duplicates that are limited to single species (D. melanogaster or Drosophila yakuba); (2) the most abundant new genes shared by multiple species (44.1%) are dispersed duplicates, and are more likely to be retained and be functional; (3) de novo gene origination from noncoding sequences plays an unexpectedly important role during the origin of new genes, and is responsible for 11.9% of the new genes; (4) retroposition is also an important mechanism, and had generated approximately 10% of the new genes; (5) approximately 30% of the new genes in the D. melanogaster species complex recruited various genomic sequences and formed chimeric gene structures, suggesting structure innovation as an important way to help fixation of new genes; and (6) the rate of the origin of new functional genes is estimated to be five to 11 genes per million years in the D. melanogaster subgroup. Finally, we survey gene frequencies among 19 globally derived strains for D. melanogaster-specific new genes and reveal that 44.4% of them show copy number polymorphisms within a population. In conclusion, we provide a panoramic picture for the origin of new genes in Drosophila species.

Figure 1.

Phylogenetic distribution of new genes. We designated numbers of new genes restricted to different lineages. Phylogenetic tree of investigated Drosophila species and their divergence times in each node are indicated (Tamura et al. 2004).

Figure 2.

Quantification of contributions to new gene origination from different mechanisms. (D. mel) D. melanogaster, (D. sch) D. sechellia, (D. sim) D. simulans. These three species together stand for the D. melanogaster species complex. We didn’t identify new genes originating from retroposition or de novo processes in the D. yakuba (D. yak) lineage due to the lack of reliable annotations in this species.

Figure 3.

Decrease of proportion of complete duplicated new genes with time. (D. mel) D. melanogaster, (D. sch) D. sechellia, (D. sim) D. simulans. These three species together stand for the D. melanogaster species complex. We compared structures and lengths of parental and new genes in D. melanogaster and the D. melanogaster species complex. New genes completely duplicating their ancestors’ coding regions seem more vulnerable to subsequent loss or structure changes during evolution.

Figure 4.

Chromosomal distribution of new genes in three datasets. New gene numbers were divided by total gene numbers on the specific chromosome as a normalization. We marked significant (*P < 0.01, Fisher’s exact test) and highly significant (**P < 0.001) overrepresentation with of new genes on certain chromosomes. We didn’t take chromosome 4 into account given the extremely low gene number on this chromosome.