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.

Figure 1

Ultrametric tree with branch lengths in millions of years for Leptinotarsa decemlineata relative to five other Coleoptera genomes. The L. decemlineata lineage is shown in orange. Branches are labeled with their length in years (top) and with the number of gene family expansions (blue) and contractions (purple) that occurred on that lineage. Rapid changes for both types are in parentheses.

Figure 2

Heatmap distribution of the abundance of transcription factor families in Leptinotarsa decemlineata compared to other insects. Each entry indicates the number of TF genes for the given family per genome, based on presence of predicted DNA binding domains. Color scale is log (base 2) and the key is depicted at the top (light blue means the TF family is completely absent). Families discussed in the main text are indicated by arrows.

Figure 3

Volcano plots showing statistically significant gene expression differences after Bonferroni correction in Leptinotarsa decemlineata. (A) Mid -gut tissue versus whole larvae, (B) an adult male versus an adult female, (C) an adult male versus whole larvae, and (D) an adult female versus whole larvae. Points outside the gray area indicate >100-fold-differences in expression. Blue points indicate down-regulated genes and red points indicate up-regulated genes in each contrast.

Figure 4

Population genetic relationships and relative rates of genetic drift among Leptinotarsa decemlineata pest populations based on single nucleotide polymorphism data. Population codes: NJ- New Jersey lab strain, WIs- imidacloprid susceptible population from Arlington, Wisconsin, WIr- imidacloprid resistant population from Hancock, Wisconsin, MI- imidacloprid resistant population from Michigan, and EU- European samples combined from Italy and Russia.

Figure 5

Phylogenetic relationships of the cysteine peptidase gene family in Leptinotarsa decemlineata compared to model insects. Species abbreviations are: L. decemlineata (Ld, green color), Drosophila melanogaster (Dm, blue color), Apis mellifera (Am, purple color), and Tribolium castaneum (Tc, red color). Mid-gut gene expression (TPM) of highly expressed L. decemlineata cysteine peptidases is shown as bar graphs across three replicate treatments.