Molecular evolution in the Drosophila melanogaster species subgroup: frequent parameter fluctuations on the timescale of molecular divergence

Abstract

Although mutation, genetic drift, and natural selection are well established as determinants of genome evolution, the importance (frequency and magnitude) of parameter fluctuations in molecular evolution is less understood. DNA sequence comparisons among closely related species allow specific substitutions to be assigned to lineages on a phylogenetic tree. In this study, we compare patterns of codon usage and protein evolution in 22 genes (>11,000 codons) among Drosophila melanogaster and five relatives within the D. melanogaster subgroup. We assign changes to eight lineages using a maximum-likelihood approach to infer ancestral states. Uncertainty in ancestral reconstructions is taken into account, at least to some extent, by weighting reconstructions by their posterior probabilities. Four of the eight lineages show potentially genomewide departures from equilibrium synonymous codon usage; three are decreasing and one is increasing in major codon usage. Several of these departures are consistent with lineage-specific changes in selection intensity (selection coefficients scaled to effective population size) at silent sites. Intron base composition and rates and patterns of protein evolution are also heterogeneous among these lineages. The magnitude of forces governing silent, intron, and protein evolution appears to have varied frequently, and in a lineage-specific manner, within the D. melanogaster subgroup.

Figure 1.

Phylogenetic relationships within the melanogaster subgroup. Unrooted synonymous distance tree of species in the melanogaster group. Silent distances, d_s, were calculated individually for Adh, Adhr, Gld, and ry genes using CODEML (F3×4 model; Yang 1997). Branch lengths are the averages of silent distances across these four genes (×1000). The D. melanogaster subgroup is boxed. All nodes within the subgroup were supported with 100% bootstrap scores for neighbor-joining, parsimony, and ML methods (Ko et al. 2003). Abbreviations for species (that are not given in Table 2) are: eug, D. eugracilis; mim, D. mimetica; lut, D. lutescens; ana, D. ananassae; pse, D. pseudoobscura; and sub, D. subobscura (pse and sub are employed as outgroups). Branch lengths, d_s, are shown except for lineages within the melanogaster subgroup species: mel (0.073), sim (0.052), tei (0.076), yak (0.050), ere (0.063), ore (0.053), melsim (0.061), teiyak (0.077), ereore (0.056), and teiyakereore (0.042). Lineages are named according to the most recent node (i.e., melsim refers to the lineage from the common ancestor of the subgroup to the common ancestor of D. melanogaster and D. simulans).

Figure 2.

Lineage-specific silent evolution in the D. melanogaster subgroup. For each lineage, counts of unpreferred and preferred silent changes are shown for each gene. Data are plotted in the histograms in decreasing order of (up − pu) for each lineage. The transition from positive to negative values is marked with a dotted line on each graph. Abbreviations for lineages are given in Table 2.

Figure 3.

Nonstationary base composition in the D. melanogaster subgroup. Differences in the percentage of SW and WS changes, d_WS,SW, are shown for MCU_H, MCU_L, introns, and replacement changes for lineages in the D. melanogaster subgroup. Data and statistical analyses are given in Table 4.

Figure 4.

Molecular distances among lineages in the D. melanogaster subgroup. (A) Relative distances for silent changes within MCU_H and MCU_L regions, changes in introns, and replacement changes are shown for lineages within the D. melanogaster subgroup. For each class, the number of changes within each lineage is divided by the total for eight lineages. (B) Scaled protein distance among lineages within the D. melanogaster subgroup. Relative protein distances are scaled by silent distances in MCU_H and MCU_L regions and by intron distances.