Abstract

The key to the coexistence of two or more species on the same host is ecological niche separation. Adult Eucryptorrhynchus scrobiculatus and E. brandti both feed on the tree of heaven, Ailanthus altissima, but on different sections of the plant. Olfaction plays a vital role in foraging for food resources. Chemosensory genes on the antennae, the main organ for insect olfaction, might explain their feeding differentiation. In the present study, we identified 130 and 129 putative chemosensory genes in E. scrobiculatus and E. brandti, respectively, by antennal transcriptome sequencing, including 31 odorant-binding proteins (OBPs), 11 chemosensory proteins (CSPs), 49 odorant receptors (ORs), 17 ionotropic receptors (IRs), 19 gustatory receptors (GRs), and three sensory neuron membrane proteins (SNMPs) in E. scrobiculatus and 28 OBPs, 11 CSPs, 45 ORs, 25 IRs, 17 GRs, and three SNMPs in E. brandti. We inferred that EscrOBP8 (EscrPBP1), EscrOBP24 (EscrPBP2) and EbraOBP8 (EbraPBP1), EbraOBP24 (EbraPBP2) were putative PBPs by the phylogenetic analysis. We identified species-specific OR transcripts (10 EscrORs and 8 EbraORs) with potential roles in the recognition of specific volatiles of A. altissima. In addition to conserved “antennal IRs,” we also found several “divergent IRs” orthologues in E. scrobiculatus and E. brandti, such as EscrIR16, EbraIR19, and EbraIR20. Compared with other chemosensory genes, GRs between E. scrobiculatus and E. brandti shared lower amino acid identities, which could explain the different feeding habits of the species. We examined OBP expression patterns in various tissues and sexes. Although amino acid sequence similarities were high between EscrOBPs and EbraOBPs, the homologous OBPs showed different tissue expression pattern between two weevils. Our systematic comparison of chemosensory genes in E. scrobiculatus and E. brandti provides a foundation for studies of olfaction and olfactory differentiation in the two weevils as well as a theoretical basis for studying species differentiation.

Highlights

  • Over a long period of evolution, phytophagous insects and their hosts have formed a complete system of co-evolution

  • We sequenced the transcriptomes of female antennae (FA) and male antennae (MA) of E. scrobiculatus and E. brandti with three independent biological replicates

  • We analyzed the antennal transcriptomes of E. scrobiculatus and E. brandti and searched for chemosensory genes to evaluate interspecific differences in olfactory genes

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Summary

Introduction

Over a long period of evolution, phytophagous insects and their hosts have formed a complete system of co-evolution. For two or more species living on the same host plant with a similar niche, competition over food resources is inevitable; only differentiation in time, space, or nutrition can reduce interspecific competition and enable coexistence. Eucryptorrhynchus scrobiculatus Motschulsky and E. brandti (Harold) (Coleoptera: Curculionidae) are sympatric, closely related species native to China and are highly hostspecific, feeding on the tree of heaven, Ailanthus altissima (Mill.) Swingle, and its variant A. altissima var. The mixed cooccurrence of E. scrobiculatus and E. brandti results in extensive A. altissima deaths in the Ningxia Hui autonomous region (Hu et al, 2012; Yu et al, 2012). The coexistence of E. scrobiculatus and E. brandti can be explained by significant differentiation of trophic niches; E. scrobiculatus adults feed on 1-year-old branches, perennial branches, and petioles, while E. brandti adults feed on the stem of A. altissima (Ji et al, 2017). The role of olfaction in their feeding differentiation is unknown

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