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

Abstract

Background Olfaction 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. Results We 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 GRs was limited in D. ponderosae and apparently absent in A. planipennis, which also has 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 OBPs, a novel OBP “tetramer”, and as many as eleven IR75 members. Simple orthology was generally rare, but we report one clade of orthologous putative bitter-taste GRs (named the “GR215 clade”), and conservation of IR60a from Drosophila melanogaster also in beetles. Conclusions Our annotation represents significant quantitative and qualitative improvements compared to original datasets derived from transcriptomes of D. ponderosae and A. planipennis. These gene sets facilitate evolutionary analysis of chemosensory genes in the Coleoptera where only a few genomes were annotated previously, and 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 destructive pests.

The draft genome of the specialist flea beetle Altica viridicyanea (Coleoptera: Chrysomelidae) provides insight into host plant specialization

“…In contrast, the gene number is greater than the oligophagous Agrilus planipennis (132 genes and two pseudogenes), but smaller than other oligophagous species such as Dendroctonus ponderosae (240 genes plus 10 pseudogenes) and L. decemlineata (> 300 genes) (Table S5). These ndings generally support the hypothesis that chemosensory gene content and host speci city should correlate in phytophagous beetles [52].…”

“…Interestingly, we also found a large expansion in A. viridicyanea in Group 4 that contained 17 ORs. By comparison, no more than four Group 4 OR genes have been previously identi ed in any other surveyed beetle species [52,55].…”

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

“…GRs detect nonvolatile chemicals and contribute to the detection of carbon dioxide (Jones et al, 2007;Robertson and Kent, 2009), whereas the olfactory antennal IRs are associated with the detection of mainly acids and amines Min et al, 2013). However, the ORs are believed to be the primary mechanism by which insects recognize volatile compounds (Fleischer et al, 2018), and thus are frequently studied as links between ecological specialization, adaptation and gene family evolution (Andersson et al, 2019). Their rapid evolution can in turn inform models of multigene family evolution, a fundamental problem of evolutionary biology (Benton, 2015).…”

“…The OR family evolved from a lineage of GRs (Robertson et al, 2003), and the few comprehensive functional analyses suggest that each receptor includes a unique ligand binding site that varies in its specificity (reviewed in Andersson et al, 2019). Together with the olfactory receptor coreceptor (Orco), these 'specific ORs' form a heterotetrameric receptor complex (Butterwick et al, 2018) in the membrane of olfactory sensory neurones.…”

“…These studies illustrate a second complication of OR evolution, which is the pattern of rapid gain and loss. This birth-anddeath model (Nei et al, 2008) presumably is tracking each species' divergence in olfactory ecology, which could be variously attributed to diet breadth, sociality, or a capacity for olfactory memory (Andersson et al, 2019). Regardless, the outcome is a labyrinthine phylogeny that frequently lacks resolution or support at its higher-level nodes (Engsontia et al, 2014;Zhou et al, 2015).…”