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.

Highlights

  • The Colorado potato beetle is one of the most challenging agricultural pests to manage

  • The draft genome assembly of L. decemlineata is 1.17 Gb and consists of 24,393 scaffolds, with a N50 of 414 kb and a contig N50 of 4.9 kb. This assembly is more than twice the estimated genome size of 460 Mb56, with the presence of gaps comprising 492 Mb, or 42%, of the assembly. As this size might be driven by underlying heterozygosity, we performed scaffolding with REDUNDANS57, which reduced the assembly size to 642 Mb, with gaps reduced to 1.3% of the assembly

  • We found that gene expansion of cysteine cathepsins from the C1 family in L. decemlineata correlates with the acquisition of greater digestive function by this group of peptidases, which is supported by gene expression activity of these genes in mid-gut tissue (Fig. 3A, Fig. 5)

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Summary

Introduction

The Colorado potato beetle is one of the most challenging agricultural pests to manage. The Colorado potato beetle, Leptinotarsa decemlineata Say 1824 (Coleoptera: Chrysomelidae), is widely considered one of the world’s most successful globally-invasive insect herbivores, with costs of ongoing management reaching tens of millions of dollars annually[1] and projected costs if unmanaged reaching billions of dollars[2]. This beetle was first identified as a pest in 1859 in the Midwestern United States, after it expanded from its native host plant, Solanum rostratum (Solanaceae), onto potato (S. tuberosum)[3]. It has achieved the broadest host range amongst its congeners (including, but not limited to: buffalobur (S. rostratum), potato (S. tuberosum), eggplant (S. melongena), silverleaf nightshade (S. elaeagnifolium), horsenettle (S. carolinense), bittersweet nightshade (S. dulcamara), tomato (S. lycopersicum), and tobacco (Nicotiana tabacum))[17,22,25], and exhibits geographical variation in the use of locally abundant Solanum species[26]

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