Genomic content of chemosensory genes correlates with host range in wood-boring beetles (Dendroctonus ponderosae, Agrilus planipennis, and Anoplophora glabripennis)

Martin N Andersson,Christopher I Keeling,Robert F Mitchell

doi:10.1186/s12864-019-6054-x

Abstract

BackgroundOlfaction and gustation underlie behaviors that are crucial for insect fitness, such as host and mate selection. The detection of semiochemicals is mediated via proteins from large and rapidly evolving chemosensory gene families; however, the links between a species’ ecology and the diversification of these genes remain poorly understood. Hence, we annotated the chemosensory genes from genomes of select wood-boring coleopterans, and compared the gene repertoires from stenophagous species with those from polyphagous species.ResultsWe annotated 86 odorant receptors (ORs), 60 gustatory receptors (GRs), 57 ionotropic receptors (IRs), 4 sensory neuron membrane proteins (SNMPs), 36 odorant binding proteins (OBPs), and 11 chemosensory proteins (CSPs) in the mountain pine beetle (Dendroctonus ponderosae), and 47 ORs, 30 GRs, 31 IRs, 4 SNMPs, 12 OBPs, and 14 CSPs in the emerald ash borer (Agrilus planipennis). Four SNMPs and 17 CSPs were annotated in the polyphagous wood-borer Anoplophora glabripennis. The gene repertoires in the stenophagous D. ponderosae and A. planipennis are reduced compared with those in the polyphagous A. glabripennis and T. castaneum, which is largely manifested through small gene lineage expansions and entire lineage losses. Alternative splicing of GR genes was limited in D. ponderosae and apparently absent in A. planipennis, which also seems to have lost one carbon dioxide receptor (GR1). A. planipennis has two SNMPs, which are related to SNMP3 in T. castaneum. D. ponderosae has two alternatively spliced OBP genes, a novel OBP “tetramer”, and as many as eleven IR75 members. Simple orthology was generally rare in beetles; however, we found one clade with orthologues of putative bitter-taste GRs (named the “GR215 clade”), and conservation of IR60a from Drosophila melanogaster.ConclusionsOur genome annotations represent important quantitative and qualitative improvements of the original datasets derived from transcriptomes of D. ponderosae and A. planipennis, facilitating evolutionary analysis of chemosensory genes in the Coleoptera where only a few genomes were previously annotated. Our analysis suggests a correlation between chemosensory gene content and host specificity in beetles. Future studies should include additional species to consolidate this correlation, and functionally characterize identified proteins as an important step towards improved control of these pests.

Highlights

Olfaction and gustation underlie behaviors that are crucial for insect fitness, such as host and mate selection
Ten of the original gene models were discarded: one Odorant receptor (OR) gene was the result of a transcript chimera; one Ionotropic receptor (IR) gene showed no homology to insect IRs; two IR gene fragments were dropped because they were revealed to belong to the same genes as two other previously reported partial IR genes; one IR gene, four Odorant binding protein (OBP) genes, and one chemosensory protein (CSP) gene were assembly isoforms or alleles of other genes (Additional file 2: Table S2)
The total numbers of such genes in the Pinus specialist D. ponderosae and the Fraxinus specialist A. planipennis are lower than in T. castaneum and A. glabripennis (Table 1). This was consistent across all chemosensory gene families, with especially large differences observed among the ORs, Gustatory receptor (GR), and IRs, followed by the OBPs, especially in A. planipennis

Summary

Introduction

Olfaction and gustation underlie behaviors that are crucial for insect fitness, such as host and mate selection. The chemical senses –olfaction and taste– underlie the ability to find mates, food, and oviposition sites, and to avoid harmful situations and non-host habitats [1]. Understanding the ‘birth-and-death’ evolution of these genes is needed to gain insight into the mechanisms underlying ecological specialization, evolutionary divergence, and speciation [2, 3], and it may reveal molecular targets that can be manipulated for insect control, such as pheromone receptors [4]. The aim was to investigate how their host breadth (stenophagy vs polyphagy) may correlate with the diversification of genomic repertoires of chemosensory genes, and at the same time reveal genes that can be targeted for improved control of these forest pests [4]

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Conclusion