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.comparative genomics ͉ gustatory receptor ͉ host adaptation ͉ lineage-specific ͉ olfactory receptor H ost specialization and host shifts in insects that feed on plants provide excellent opportunities to study the genetic basis of ecological adaptation. Until now, however, this endeavor has been limited to attempts to map factors responsible for conspicuous phenotypic changes that accompany the ecological shifts (e.g., refs. 1-5). We know nothing about genetic changes whose individual effects are subtle, but whose combined presence may leave a striking signature on the genomes of specializing or host-shifting insects.For example, insects evaluate their environment largely by smell and taste, and we might therefore expect their chemical sensory systems to evolve during host specialization or shifts. The acquisition of a novel host may drive the adaptive divergence of sensory systems by positive selection, and the abandonment of an ancestral host may result in the deterioration of older sensory adaptations by genetic drift (or positive selection). Despite their potentially subtle phenotypic effects, such changes are likely to be pervasive (particularly because new host plants challenge insects with the task of recognizing and responding not only to a new food but often also to novel toxins, bacteria, fungi, predators, parasitoids, pupation sites, and mating environments) and are best detected by examining entire genomes or large groups of genes simultaneously.The olfactory receptor (Or) and gustatory receptor (Gr) gene families encode a diverse group of transmembrane proteins that bind volatile and soluble chemicals from the environment and trigger nerve impulses to the brain (6). Individual receptor genes in insects are highly divergent (paralogous genes from a single species often sharing Ͻ20% of their amino acids), are expressed in narrow subsets of olfactory and gustatory neurons from well defined regions of smell and taste organs, and la...

When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses

“…An ongoing process of pseudogenization was also observed for copies corresponding to different ptp genes in different species [60]. As shown in primates, Drosophila or large DNA viruses such as poxviruses, gene expansion and contraction could explain important adaptive traits allowing physiological adaptations of their host species [91][92][93]. The expansion of the ptp gene family could therefore be an important source of evolutionary innovations conferring new adaptive traits to the wasps.…”

Evolution of genes and genomes on the Drosophila phylogeny

“…Generalists are expected to encounter the most diverse set of tastants and seem to have maintained the greatest diversity of gustatory receptors. Second, Or and Gr genes that remain intact in D. sechellia and D. erecta evolve significantly more rapidly along these two lineages (v 5 0.1556 for Ors and 0.1874 for Grs) than along the generalist lineages (v 5 0.1049 for Ors and 0.1658 for Grs; paired Wilcoxon, P 5 0.0003 and 0.003, respectively 124 ). There is some evidence that odorant-binding protein genes also evolve significantly faster in specialists compared to generalists 122 .…”

“…Furthermore, clear lineagespecific differences are detectable between generalist and specialist species within the melanogaster subgroup. First, the two independently evolved specialists (D. sechellia and D. erecta) are losing Gr genes approximately five times more rapidly than the generalist species 121,124 . We believe this result is robust to sequence quality, because all pseudogenes and deletions were verified by direct re-sequencing and synteny-based orthologue searches, respectively.…”

Molecular evolution of the major chemosensory gene families in insects

“…The putative functional diversification associated with such sequence divergence has been studied by comparative analysis of synonymous (d S ) and non- (Forêt and Maleszka 2006;Guo and Kim, 2007;McBride, 2007;McBride and Arguello, 2007;Vieira et al, 2007;Gardiner et al, 2008). This widely used and powerful approach allows the inference of the selective pressure on protein coding sequences, and it also allows several competitive evolutionary scenarios to be explored and tested.…”