Genomic Content of Chemosensory Receptors in Two Sister Blister Beetles Facilitates Characterization of Chemosensory Evolution

Background: More than 2500 species belong to the Meloidae family (Coleoptera: Tenebrionoidea), members of which produce the potent defensive blistering agent cantharidin and are commonly known as blister beetles or Spanishflies. Cantharidin has recently been used for cancer therapy. Hycleus cichorii and Hycleus phaleratus have been used in traditional Chinese medicine for more than 2000 years due to their ability to biosynthesize cantharidin. To understand the role of the chemosensory system in beetle evolution, we comparatively analysed the chemosensory receptor families of both blister beetle species and compared them with those of other beetles.

Results: We identified 89 odorant receptors (ORs), 86 gustatory receptors (GRs), and 45 ionotropic receptors (IRs) in H. phaleratus and 149 ORs, 102 GRs and 50 IRs in H. cichorii. Nine groups of beetle ORs were recovered, and a similar pattern of ORs in Coleoptera emerged. Two evident expanded clades in Hycleus (Groups 5A and 3) were reconstructed in the phylogenetic tree. Four of eight genes with evidence of positive selection were clustered in the expanded clades of Group 5A. Three, eight and three orthologous pairs of CO, sugar and fructose receptors, respectively, were identified in both blister beetles. Two evident expanded clades of putative bitter GRs in Hycleus were also found, and the GR in one clade had notably low divergence. Interestingly, IR41a was specifically expanded in blister beetles compared to other insects identified to date, and IR75 was also clearly expanded in both blister beetles based on our phylogenetic tree analysis. Moreover, evidence of positive selection was detected for eight ORs, three GRs and two IRs, half of which were from five duplicate clades.

Conclusions: We first annotated the chemosensory receptor families in a pair of sister beetle genomes (Meloidae: Hycleus), which facilitated evolutionary analysis of chemosensory receptors between sibling species in the Coleoptera group. Our analysis suggests that changes in chemosensory receptors have a possible role in chemical-based species evolution in blister beetles. Future studies should include more species to verify this correlation, which will help us understand the evolution of blister beetles.