Elevated rates of positive selection drive the evolution of pestiferousness in the Colorado potato beetle (Leptinotarsa decemlineata, Say)

Abstract

Insect pests are characterized by expansion, preference and performance on agricultural crops, high fecundity and rapid adaptation to control methods, which we collectively refer to as pestiferousness. Which organismal traits and evolutionary processes facilitate certain taxa becoming pests remains an outstanding question for evolutionary biologists. In order to understand these features, we set out to test the relative importance of genomic properties that underlie the rapid evolution of pestiferousness in the emerging pest model: the Colorado potato beetle (CPB), Leptinotarsa decemlineata Say. Within the Leptinotarsa genus, only CPB has risen to pest status on cultivated Solanum. Using whole genomes from ten closely related Leptinotarsa species, we reconstructed a high-quality species tree of this genus. Within this phylogenetic framework, we tested the relative importance of four drivers of rapid adaptation: standing genetic variation, gene family expansion and contraction, transposable element variation, and protein evolution. Throughout approximately 20 million years of divergence, Leptinotarsa show little evidence of gene family turnover or transposable element variation contributing to pest evolution. However, there is a clear pattern of pest lineages experiencing greater rates of positive selection on protein coding genes, as well as retaining higher levels of standing genetic variation. We also identify a suite of positively selected genes unique to the Colorado potato beetle that are directly associated with pestiferousness. These genes are involved in xenobiotic detoxification, chemosensation, and hormones linked with pest behavior and physiology.