Accelerated sequence divergence of conserved genomic elements in Drosophila melanogaster

Abstract

Recent genomic sequencing of 10 additional Drosophila genomes provides a rich resource for comparative genomics analyses aimed at understanding the similarities and differences between species and between Drosophila and mammals. Using a phylogenetic approach, we identified 64 genomic elements that have been highly conserved over most of the Drosophila tree, but that have experienced a recent burst of evolution along the Drosophila melanogaster lineage. Compared to similarly defined elements in humans, these regions of rapid lineage-specific evolution in Drosophila differ dramatically in location, mechanism of evolution, and functional properties of associated genes. Notably, the majority reside in protein-coding regions and primarily result from rapid adaptive synonymous site evolution. In fact, adaptive evolution appears to be driving substitutions to unpreferred codons. Our analysis also highlights interesting noncoding genomic regions, such as regulatory regions in the gene gooseberry-neuro and a putative novel miRNA.

Figure 1.

(A) Phylogeny of 11 Drosophila species with genome sequences. Branch lengths are derived from maximum likelihood analysis of all elements conserved throughout the tree. Branches in blue (D. simulans, D. yakuba, and D. erecta) were used to identify the blocks of at least 100 bp with 96% identity between the three species. All other lineages (and the D. melanogaster–D. simulans ancestor) were used to infer whether D. melanogaster had an accelerated rate of evolution relative to the expected rate of evolution based on elements conserved throughout the tree. (B) Locations of D. melanogaster accelerated regions (DMARs). (Stacked bars) Multiple DMARs within a single locus. (Two bars above a “V”) Two DMARs that were within the same chromosomal band. DMARs are found predominately in exons (46/64) and are significantly over-represented on the X chromosome (16/64). Chromosome images adapted from Lefevre (1976).

Figure 2.

Nonsynonymous (A) and synonymous (B) substitution rates for DMARs in coding regions and the genes that contain those DMARs. Rates are per nonsynonymous site or synonymous site. Both DMAR_SS and the genes that contain them (light gray and white bars) have very low levels of amino acid divergence. (Black and dark gray bars) DMAR_AA have high rates of synonymous and nonsynonymous substitution, but the genes that contain them evolve at similar rates to the genomic average (dashed line).