Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia

Abstract

Our understanding of the genetic basis of host specialization in insects is limited to basic information on the number and location of genetic factors underlying changes in conspicuous phenotypes. We know nothing about general patterns of molecular evolution that may accompany host specialization but are not traceable to a single prominent phenotypic change. Here, I describe changes in the entire repertoire of 136 olfactory receptor (Or) and gustatory receptor (Gr) genes of the recently specialized vinegar fly Drosophila sechellia. I find that D. sechellia is losing Or and Gr genes nearly 10 times faster than its generalist sibling Drosophila simulans. Moreover, those D. sechellia receptors that remain intact have fixed amino acid replacement mutations at a higher rate relative to silent mutations than have their D. simulans orthologs. Comparison of these patterns with those observed in a random sample of genes indicates that the changes at Or and Gr loci are likely to reflect positive selection and/or relaxed constraint associated with the altered ecological niche of this fly.

Fig. 1.

Phylogenetic relationships among D. sechellia, D. simulans, and D. melanogaster. D. sechellia is a specialist, whereas D. simulans is a generalist. I compare the molecular evolution of Or and Gr genes along these two lineages (branches a and b) using D. melanogaster as an outgroup. Divergence times are from refs. and .

Fig. 2.

Distribution of the difference in Ka/Ks between the D. sechellia and D. simulans lineages for each pair of orthologous receptor genes (red stripes) and control genes (black stripes). Note that both distributions are shifted to the right of the solid black line at zero (indicating that Ka/Ks tends to be higher in D. sechellia than in D. simulans), but that the distribution for receptors is shifted further to the right than that for controls.