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 spider mite, Tetranychus urticae, an extreme generalist. Strikingly, T. urticae has more CRs than reported in any other arthropod to date. Including pseudogenes, 689 gustatory receptors were identified, as were 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. Although pseudogenization of many gustatory receptors within clusters suggests relaxed selection, a subset of receptors is expressed. Consistent with functions as CRs, the genomic distribution and expression of ENaCs in lineage-specific T. urticae expansions mirrors that observed for gustatory receptors. The expansion of ENaCs in T. urticae to > 3-fold that reported in other animals was unexpected, raising the possibility that ENaCs in T. urticae have been co-opted to fulfill a major 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.

Varroa chemosensory proteins: some are conserved across Arthropoda but others are arachnid specific

“…The absence of ORs is consistent with former studies on non-insect arthropods, and further augments the hypothesis that this group of chemoreceptors evolved after the split of Insecta and Crustacea (470 million years ago), and is unique to insects (Grbic et al, 2007;Peñalva-Arana et al, 2009;Chipman et al, 2014;Hoy et al, 2016;Ngoc et al, 2016;Vizueta et al, 2016). However, no transcripts that contained OR or CSP domains were detected.…”

“…Recently, IR genes were reported for several other arachnids, including Tetranychus urticae (Ngoc et al, 2016), G. occidentalis (Hoy et al, 2016), Tropilaelaps mercedesae (Dong et al, 2017) and the spider D. silvatica (Vizueta et al, 2016). However, only 13 of them contained at least two of the essential domains.…”

“…Recently, a high number of ENaC genes were identified in the genomes of T. urticae, G. occidentalis and I. scapularis (Ngoc et al, 2016). Interestingly, all upregulated transcripts are clustered together in the phylogenetic analysis, along with other arachnid sequences, whereas transcripts not exhibiting differential expression clustered closer to D. melanogaster ENaCs.…”

“…Regarding membrane-bound proteins and receptors, all of the potential chemoreceptors found in Chelicerata to date belong to the ion-gated channel receptor groups with the exception of potential G-protein coupled receptors (GPCRs) found in the forelegs of the dog tick Dermacentor variabilis (Carr and Roe, 2016), resembling odorant receptors (ORs) identified to date only in insects. The identified chemoreceptor homologues in Chelicerata include members of potential olfactory ionotropic receptors (IRs), gustatory receptors (GRs) (Eyun et al, 2017) and the more divergent degenerin/epithelial Na+ channel (ENaC) family as well as the transient receptor potential (TRP) family (Ngoc et al, 2016).…”

“…Olfactory IRs belonging to the ionotropic glutamate receptor (IGR) superfamily can be found across all protostomes and are implicated as ancient chemoreceptors (Croset et al, 2010;Rytz et al, 2013). Orthologues of the Drosophila melanogaster ionotropic receptor IR25a, which acts as an IR co-receptor, as well as orthologues of glutamate receptors (GRs), have been reported in some Acari, Araneae (Croset et al, 2010;Gulia-Nuss et al, 2016;Hoy et al, 2016;Ngoc et al, 2016;Vizueta et al, 2016;Dong et al, 2017), as well as in Crustacea (Daphnia pulex; Peñalva-Arana et al, 2009;Croset et al, 2010). The ion channel receptor families of ENaCs and TRPs are considered as important receptors for the perception of both outer and inner environments, including chemoperception (Venkatachalam and Montell, 2007;Ben-Shahar, 2011;Zelle et al, 2013;Peng, Shi, et al, 2015).…”