A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

Abstract

The Colorado potato beetle is one of the most challenging agricultural pests to manage. It has shown a spectacular ability to adapt to a variety of solanaceaeous plants and variable climates during its global invasion, and, notably, to rapidly evolve insecticide resistance. To examine evidence of rapid evolutionary change, and to understand the genetic basis of herbivory and insecticide resistance, we tested for structural and functional genomic changes relative to other arthropod species using genome sequencing, transcriptomics, and community annotation. Two factors that might facilitate rapid evolutionary change include transposable elements, which comprise at least 17% of the genome and are rapidly evolving compared to other Coleoptera, and high levels of nucleotide diversity in rapidly growing pest populations. Adaptations to plant feeding are evident in gene expansions and differential expression of digestive enzymes in gut tissues, as well as expansions of gustatory receptors for bitter tasting. Surprisingly, the suite of genes involved in insecticide resistance is similar to other beetles. Finally, duplications in the RNAi pathway might explain why Leptinotarsa decemlineata has high sensitivity to dsRNA. The L. decemlineata genome provides opportunities to investigate a broad range of phenotypes and to develop sustainable methods to control this widely successful pest.

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

“…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.…”

“…We built a preliminary set of gene models by searching each genome with BLAST queries of the published ORs from T. castaneum , An. glabripennis , L. decemlineata , D. ponderosae and Ips typographus L. (Engsontia et al ., ; Andersson et al ., ; McKenna et al ., ; Schoville et al ., ). We in turn used these initial models as additional queries, and this process was repeated to iteratively search the genomes until novel hits were exhausted.…”

“…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).…”

“…Some confusion stems from limited genomic annotation, because ORs are represented in most insect orders by the one or few exemplar species for which genomic sequences are available (summarized in Robertson, ). Transcriptomes are numerous, but generally do not describe the full suite of receptors owing to low and/or spatiotemporal expression of some OR genes (eg Liu et al ., vs. Schoville et al ., ). Some orders such as the Diptera, Lepidoptera and Hymenoptera have received a more detailed treatment that compares genomes of several genera or families (Gardiner et al ., ; Engsontia et al ., ; Zhou et al ., ).…”

“…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).…”