The diversity and evolution of odorant receptors in beetles (Coleoptera)

Abstract

The insect odorant receptors (ORs) are amongst the largest gene families in insect genomes and the primary means by which insects recognize volatile compounds. The evolution of ORs is thus instrumental in explaining the chemical ecology of insects and as a model of evolutionary biology. However, although ORs have been described from numerous insect species, their analysis within and amongst the insect orders has been hindered by a combination of limited genomic information and a tendency of the OR family toward rapid divergence, gain, and loss. We addressed these issues in the insect order Coleoptera through a targeted genomic annotation effort that included 1181 ORs from one species of the sister order Strepsiptera and 10 species representing the four coleopteran suborders. The numbers of ORs in each species varied from hundreds to fewer than 10, but coleopteran ORs could nevertheless be represented within a scheme of nine monophyletic subfamilies. We observed many radiations and losses of genes amongst OR subfamilies, and the diversity of ORs appeared to parallel the host breadth of the study species. However, some small lineages of ORs persisted amongst many coleopteran families, suggesting receptors of key function that underlie the olfactory ecology of beetles.

Putative ligand binding sites of two functionally characterized bark beetle odorant receptors

“…Additionally, I. typographus lacked ORs in groups 3, 4, 5B, and 6, which is also true for D. ponderosae. In contrast to previous studies 39,40 , our tree did not recapitulate the monophyly of OR group 2, with the two group 4 OR members from the cerambycid Anoplophora glabripennis being associated with the 2B group. This discrepancy is likely explained by the limited number of group 4 ORs in the analysis, in combination with the comparatively low node support for the 2A/2B distinction observed previously 39 .…”

“…In contrast to previous studies 39,40 , our tree did not recapitulate the monophyly of OR group 2, with the two group 4 OR members from the cerambycid Anoplophora glabripennis being associated with the 2B group. This discrepancy is likely explained by the limited number of group 4 ORs in the analysis, in combination with the comparatively low node support for the 2A/2B distinction observed previously 39 . Our analysis also indicated the presence of 19 simple 1:1 orthologous relationships between ItypORs and DponORs of which 17 have high bootstrap support (³90%; Figure 1).…”

“…The number of ORs (73) in the I. typographus transcriptome is close to the number of putatively functional ORs (79) in the genome of the mountain pine beetle D. ponderosae 39 , and clearly higher compared to previous analyses of antennal transcriptomes of this and other species of bark beetles 38,49 , suggesting a good coverage of our analysis. The larger number of ORs compared to the original ItypOR dataset is likely due to improved sequencing depth and methodology 38 .…”

“…The larger number of ORs compared to the original ItypOR dataset is likely due to improved sequencing depth and methodology 38 . A recent phylogenetic analysis of ORs from ten species across the Coleoptera identified nine major OR clades 39 . It showed that OR lineage radiations and losses among the nine clades differ remarkably between taxa, but also that OR distributions are more similar between closely related beetle families.…”

“…A recent study defined nine major clades of coleopteran ORs 39 . Our phylogenetic analysis of ORs from the Curculionidae and Cerambycidae families showed that the largest number of ItypORs were found in group 7 (29 ORs), followed by group 5A (21 ORs), group 1 (11 ORs), group 2A (7 ORs) and 2B (4 ORs), which is similar to the OR distribution in the other bark beetle species in the analysis, Dendroctonus ponderosae (Figure 1).…”