Olfactory and gustatory receptor genes in fig wasps: Evolutionary insights from comparative studies

Abstract

The mechanisms of chemoreception in fig wasps (Hymenoptera, Agaonidae) are of primary importance in their co-evolutionary relationship with the fig trees they pollinate. We used transcriptome sequences of 25 fig wasps in six genera that allowed a comparative approach to the evolution of key molecular components of fig wasp chemoreception: their odorant (OR) and gustatory (GR) receptor genes. In total, we identified 311 ORs and 47 GRs, with each species recording from 5 to 30 OR genes and 1-4 GR genes. 304 OR genes clustered into 18 orthologous groups known to be sensitive to cuticular hydrocarbons (CHC), pheromones, acids, alcohols and a variety of floral scents such as cineole, Linalool, and Heptanone. 45 GR genes clustered into 4 orthologous groups that contain sweet, bitter, CO₂ and undocumented receptors. Gene sequences in most orthologous groups varied greatly among species, except for ORco (60.0% conserved) and sweet receptors (30.7% conserved). Strong purifying selection of both odorant and gustatory genes was detected, as shown by low ω values. Signatures of positive selection were detected in loci from both OR and GR orthologous groups. Fig wasps have relatively few olfactory and especially gustatory receptors, reflecting the natural history of the system. Amino acid sequences nonetheless vary significantly between species and are consistent with the phylogenetic relationships among fig wasps. The differences in ORs within some orthologous groups from the same species, but different hosts and from closely related species from one host can reach as low as 49.3% and 9.8% respectively, implying the ORs of fig wasps can evolve rapidly to novel ecological environments. Our results provide a starting point for understanding the molecular basis of the chemosensory systems of fig wasps.

Keywords: Adaptation; Chemical communication; Ficus; Fig wasps; Host specificity; Mutualism.