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

<p class="Paragraph">In order to understand the evolution of pestiferousness, which we define as the accumulation of traits that contribute to an insect population's success in an agroecosystem, we tested the importance of known genomic properties associated with rapid adaptation. Within the leaf beetle genus <i>Leptinotarsa</i>, only the Colorado potato beetle (CPB), <i>Leptinotarsa decemlineata</i> Say, and a few populations therein, has risen to pest status on cultivated nightshades, <i>Solanum</i>. Using whole genomes from ten closely related <i>Leptinotarsa</i> species native to the United States we reconstructed a high-quality species tree and used this phylogenetic framework to assess evolutionary patterns in four genomic features of rapid adaptation: standing genetic variation, gene family expansion and contraction, transposable element variation, and positive selection at protein coding genes. Throughout approximately 20 million years of history, <i>Leptinotarsa</i> species show little evidence of gene family turnover and transposable element variation. However, there is a clear pattern of recently derived lineages, including CPB, experiencing higher rates of positive selection on protein coding genes. We determine these rates are associated with greater standing genetic variation due to larger effective population size, which support the theory that the demographic history contributes to rates of protein evolution. Furthermore, we identify a suite of genes under positive selection that are linked to pestiferousness, exclusively, in the Colorado potato beetle lineage. They are involved in the biological processes of xenobiotic detoxification, chemosensation, and hormone function.</p>