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

Authors: SCHOVILLE, SEAN - University Of Wisconsin; CHEN, YOLANDA - University Of Vermont; Childers, Anna; Childers, Christopher; Oppert, Brenda; Perkin, Lindsey; Poelchau, Monica; Rinehart, Joe; Yocum, George; RICHARDS, STEPHEN - Baylor College Of Medicine

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/13/2018
Publication Date: 1/31/2018
Citation: Schoville, S.D., Chen, Y.H., Childers, A.K., Childers, C., Oppert, B.S., Perkin, L.C., Poelchau, M.F., Rinehart, J.P., Yocum, G.D., Richards, S. 2018. A model species for agricultural pest genomics: the genome of the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Scientific Reports. 8(1):1931. https://doi.org/10.1038/s41598-018-20154-1.

Interpretive Summary: The Colorado potato beetle, Leptinotarsa decemlineata, is known as an “international super pest” due to the billions in dollars of damage it does to the world potato crop each year. Native to southern Mexico, this insect was first discovered in The United States in the early 1800s and adapted to feeding on potato by 1859. Since then its geographic range has expanded across the northern hemisphere and now threatens potato crops in the southern hemisphere as well. Due to the critical importance of this pest, and as a component of the USDA-ARS i5k initiative, a consortium of federal and university researchers sequenced its genome in order to develop a comprehensive understanding of its biological mechanisms. Our initial studies have focused on three main characteristics that have enabled the Colorado potato beetle’s rapid increase in geographic distribution: 1) the ability to adapt to feeding on other plants within the potato family (both wild and cultivated species of the nightshade family) which enable the beetle to survive when potatoes are not available, 2) the ability to adapt to local weather conditions from the arid conditions of southern Mexico to the northern latitudes of Canada and Russia, and 3) a unique ability to develop resistance to all the major classes of insecticides, sometimes in the very first year of exposure. Analysis of the genome has given us insights into all three of these characteristics: 1) an increase in the taste receptors may account for adaptation to the bitter tasting plants in the nightshade family, 2) although this insect can adapt to wide climatic variations, no significant differences in environmental stress genes were noted, and 3) despite its notoriety in adapting to insecticides, this insect has a similar suite of genes involved in resistance compared to other beetles, indicating the Colorado potato beetle may have a novel insecticide resistance mechanism. Our initial results are encouraging, and we expect that the Colorado potato beetle genome will provide new opportunities for a deeper understanding of the ecology, evolution, and management of this species.

Technical Abstract: The Colorado potato beetle, Leptinotarsa decemlineata Say, is one of the most challenging agricultural pests to manage and has shown a spectacular ability to rapidly adapt to a broad range of solanaceaeous (nightshade/potato) plants, variable climate during its global invasion, and, most notably, an ability to rapidly evolve resistance to insecticides (over 50 different compounds in all the major classes, in some cases within the first year of use). To examine evidence of rapid evolutionary change, we tested for structural and functional genomic changes relative to other arthropod species, using whole-genome sequencing, transcriptome sequencing, and a large community-driven annotation effort. We present a 140x coverage whole genome sequence (>640 Mb in size) from a single, female Colorado potato beetle, with a reference gene set of 24,740 genes, among the largest Coleoptera genomes sequenced to date. Transposable elements comprise at least 17% of the genome, and are heavily represented in an analysis of rapidly evolving gene families compared to other beetles. Population genetic analyses suggest high levels of nucleotide diversity, local geographic structure, and evidence of recent population growth. Adaptations to plant feeding are evident in gene expansions and differential expression of digestive enzymes (e.g. cysteine peptidase genes) in gut tissues, as well as expansions of the gustatory receptors for bitter tasting plants in the nightshade family, Solanaceae. Despite its notoriety in adapting to insecticides, L. decemlineata has a similar suite of genes involved in resistance (metabolic detoxification and cuticle penetration) compared to other beetles. However, this beetle has interesting duplications in RNAi genes that might facilitate development of resistance to RNAi-based pesticides. As a representative of one the most evolutionarily diverse lineages, the L. decemlineata genome will undoubtedly provide new opportunities for deeper understanding on the ecology, evolution, and management of this species, as well as new opportunities to leverage genomic technologies to understand the genomic basis of a broad range of phenotypes and to develop sustainable methods to control this widely successful pest.