Duplication and gene conversion in the Drosophila melanogaster genome

Abstract

Using the genomic sequences of Drosophila melanogaster subgroup, the pattern of gene duplications was investigated with special attention to interlocus gene conversion. Our fine-scale analysis with careful visual inspections enabled accurate identification of a number of duplicated blocks (genomic regions). The orthologous parts of those duplicated blocks were also identified in the D. simulans and D. sechellia genomes, by which we were able to clearly classify the duplicated blocks into post- and pre-speciation blocks. We found 31 post-speciation duplicated genes, from which the rate of gene duplication (from one copy to two copies) is estimated to be 1.0 x 10(-9) per single-copy gene per year. The role of interlocus gene conversion was observed in several respects in our data: (1) synonymous divergence between a duplicated pair is overall very low. Consequently, the gene duplication rate would be seriously overestimated by counting duplicated genes with low divergence; (2) the sizes of young duplicated blocks are generally large. We postulate that the degeneration of gene conversion around the edges could explain the shrinkage of "identifiable" duplicated regions; and (3) elevated paralogous divergence is observed around the edges in many duplicated blocks, supporting our gene conversion-degeneration model. Our analysis demonstrated that gene conversion between duplicated regions is a common and genome-wide phenomenon in the Drosophila genomes, and that its role should be especially significant in the early stages of duplicated genes. Based on a population genetic prediction, we applied a new genome-scan method to test for signatures of selection for neofunctionalization and found a strong signature in a pair of transporter genes.

Figure 1. (A) Phylogenetic relationship of the five species in the D. melanogaster subgroup.

The distance is based on the nucleotide divergence at synonymous sites (K_S). Modified from Figure 2B of . (B–D) Evidence for gene conversion in the gene tree shapes. Xm and Ym represent a pair of duplicated gene in D. melanogaster, and their orthologs in D. simulans (or in D. sechellia) are denoted by Xs and Ys. See text for details.

Figure 2. The distribution of synonymous divergence between duplicated blocks in D. melanogaster.

K̅ _S is the average synonymous divergence for blocks with multiple coding genes. Post-Sp. and Pre-Sp. mean duplicates that arose after and before the speciation event of D. melanogaster and D. simulans, respectively.

Figure 3. Illustrations to describe the analysis of informative sites in the alignment of the four sequences.

(A) Example of the alignment of the four sequences. The types of informative sites are shown below the alignment: “C” and “N” are as defined in the text, and “M” represents a site that requires multiple mutations for explanation. (B) Relationships of the four sequences at type-C and type-N sites. (C) Patterns of double mutations. A double-mutated site is defined as one with a single substitution that has occurred since the speciation event in each of X and Y.

Figure 4. Decay of duplicated blocks.

(A) Length of duplicated blocks (L) vs. synonymous divergence (K_S). (B) Number of annotated genes vs. K_S. (C) Length of intervening region (I) vs. K_S.

Figure 5. Distributions of the divergence between duplicated blocks, obtained by a window analysis with size 100 bp.

(A) Pre6 block with the Bob genes. (B) Pre16 with the Amy genes.

Figure 6. Distributions of divergences and type-C and type-N sites in Pre28, including the CG18281-CG17637 gene pairs in D. melanogaster.

The orthologous divergence (d ₀) is the average of d_{Xm −Xs} and d_{Ym −Ys}.