Odorant receptors and antennal lobe morphology offer a new approach to understanding olfaction in the Asian longhorned beetle

Abstract

The Asian longhorned beetle Anoplophora glabripennis (Motchulsky) is an exotic forest pest that has repeatedly invaded North America and Europe from Asia, and has the potential to kill millions of trees and cause billions of dollars in damage. Traps baited with an attractive mixture of volatile organic compounds (VOCs) from hosts have been of limited success in monitoring invasion sites. We propose that lures might be improved through studying the olfactory system of adult beetles, especially the gene family of odorant receptors (ORs) and the structure of the antennal lobes of the brain. Here, we report identification of 132 ORs in the genome of A. glabripennis (inclusive of one Orco gene and 11 pseudogenes), some of which are orthologous to known pheromone receptors of other cerambycid beetles. We also identified three ORs that are strongly biased toward expression in the female transcriptome, and a single OR strongly biased toward males. Three-dimensional reconstruction of the antennal lobes of adults suggested a male-specific macroglomerulus and several enlarged glomeruli in females. We predict that functional characterization of ORs and glomeruli will lead to identification of key odorants in the life history of A. glabripennis that may aid in monitoring and controlling future invasions.

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

“…Additionally, six conserved lineages were identified within Groups 1, 2A and 2B (Figs i–ii, i–iv). No ligands were known for any ORs in this study, but one lineage (Group 2B.ii; Fig ) included AglaOR29, which is orthologous to the characterized pheromone receptor McarOR3 in the cerambycid Megacyllene caryae (Mitchell et al ., , ).…”

“…For example, the conserved lineage 2B.iii (Fig. ) was previously suggested as a novel subfamily of chrysomeloid‐specific ORs (Mitchell et al ., ; Schoville et al ., ) until additional genes were included here.…”

“…Finally, we obtained published sequences of OR genes from four species: the outgroup Apis mellifera L. (Hymenoptera: Apidae) (Amel; Robertson and Wanner, 2006), and the beetles T. castaneum (Tenebrionidae) (Tcas; Engsontia et al, 2008), An. glabripennis (Cerambycidae) (Agla; Mitchell et al, 2017) and L. decemlineata (Chrysomelidae) (Ldec; Schoville et al, 2018). We referenced the ORs of T. castaneum based on their original annotation, to facilitate comparison with the OR subfamilies that have already been published (Engsontia et al, 2008).…”

“…Subsequent antennal transcriptome analyses of other beetle families recognized an additional Group 7 (Mitchell et al, 2012;Andersson et al, 2013), and further potential OR subfamilies have occasionally been noted (eg Antony et al, 2016). Studies of the ORs in two more genomes, the longhorned beetle Anoplophora glabripennis (Motschulsky) (Cerambycidae) and the leaf beetle Leptinotarsa decemlineata (Say) (Chrysomelidae), resulted in additional support for some of the OR subfamilies, but also revealed potential novel lineages Mitchell et al, 2017;Schoville et al, 2018). Furthermore, our existing view of coleopteran OR phylogeny is incomplete because these three beetle genomes all belong to a single series (Cucujiformia) within the suborder Polyphaga, which itself is only one of four subordinal lineages recognized in the Coleoptera McKenna, 2017).…”

Morphological and Molecular Perspectives on the Phylogeny, Evolution, and Classification of Weevils (Coleoptera: Curculionoidea): Proceedings from the 2016 International Weevil Meeting

“…He talked briefly about the evolution of genes underlying specialized phytophagy in beetles and how this is related to the macroevolution of specialized plant feeding in weevils and other phytophagous beetles [110]. He also briefly mentioned collaborative studies to reconstruct the evolution of genes involved in color vision in beetles (e.g., [111]) and collaborative studies of olfaction in beetles (e.g., [112]). On a different note, he talked about the biodiversity crisis and specifically the loss of tropical biodiversity, with particular reference to the current status of forests in the Greater Congo Basin (http://tropicalbiology.org/congo-resolution/).…”