Complex evolutionary dynamics of massively expanded chemosensory receptor families in an extreme generalist chelicerate herbivore

Abstract

While mechanisms to detoxify plant produced, anti-herbivore compounds have been associated with plant host use by herbivores, less is known about the role of chemosensory perception in their life histories. This is especially true for generalists, including chelicerate herbivores that evolved herbivory independently from the more studied insect lineages. To shed light on chemosensory perception in a generalist herbivore,we characterized the chemosensory receptors (CRs) of the chelicerate two-spotted spidermite, Tetranychus urticae, an extreme generalist. Strikingly, T. urticae hasmoreCRs than reported in any other arthropod to date. Including pseudogenes, 689 gustatory receptorswere identified, aswere 136 degenerin/Epithelial Na+Channels (ENaCs) that have also been implicated as CRs in insects. The genomic distribution of T. urticae gustatory receptors indicates recurring bursts of lineage-specific proliferations, with the extent of receptor clusters reminiscent of those observed in the CR-rich genomes of vertebrates or C. elegans. Althoughpseudogenizationofmanygustatory receptors within clusters suggests relaxed selection, a subsetof receptors is expressed. Consistent with functions as CRs, the genomic distribution and expression of ENaCs in lineage-specific T. urticae expansions mirrors that observed forgustatory receptors.Theexpansion ofENaCsinT. urticae to>3-fold that reportedin other animalswasunexpected, raising the possibility that ENaCs in T. urticae have been co-opted to fulfill amajor role performed by unrelated CRs in other animals. More broadly, our findings suggest an elaborate role for chemosensory perception in generalist herbivores that are of key ecological and agricultural importance.