The genome and stage-specific transcriptomes of the carrot weevil, Listronotus oregonensis, reveal adaptive mechanisms for host specialisation and symbiotic interactions.

Abstract

Throughout their evolution, insects have become specialised to occupy diverse ecological niches. The carrot weevil, Listronotus oregonensis, is an important agricultural pest that exhibits a very specific host range. In this study, we characterised the genome and transcriptomes of each developmental stage of L. oregonensis and its Wolbachia endosymbiont to gain deeper knowledge of the genetic determinants controlling its biology. We annotated 14,637 genes and showed expression profiles across the developmental stages. We also compared orthologous genes between L. oregonensis and nine other species, with particular focus on chemoreceptors and detoxification genes. We identified 24 distinct odorant-binding protein genes and 41 genes for receptors involved in stimulus perception, relatively low numbers compared with other species, which would be consistent with a narrow host range. In contrast, we found a high number of detoxification genes, with significant expansion of certain gene families. Among the annotated genes, 46 were putatively acquired through horizontal gene transfer, with 17 showing strong evidence for this, including several cell-wall degrading enzymes. The phylogeny of a cytolethal distending toxin gene also suggests an initial transfer from a prokaryotic source and vertical dissemination in members of Curculionidae through recent evolution. The presence of the endosymbiotic bacterium Wolbachia (supergroup A) was confirmed in all tested L. oregonensis individuals from several regions in northeastern North America and showed very little diversity. This study enhances our understanding of the genomic, functional, and evolutionary aspects of a significant agricultural pest and makes important and useful databases available to the scientific community.