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

Abstract

Contextualizing evolutionary history and identifying genomic features of an insect that might contribute to its pest status is important in developing early detection and control tactics. 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 in the Colorado potato beetle (CPB), Leptinotarsa decemlineata Say. Within the leaf beetle genus Leptinotarsa, only CPB, and a few populations therein, has risen to pest status on cultivated nightshades, Solanum. Using whole genomes from ten closely related Leptinotarsa 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 abundance and location, and positive selection at protein-coding genes. Throughout approximately 20 million years of history, Leptinotarsa species show little evidence of gene family turnover and transposable element variation. However, there is a clear pattern of CPB experiencing higher rates of positive selection on protein-coding genes. We determine that these rates are associated with greater standing genetic variation due to larger effective population size, which supports the theory that the demographic history contributes to rates of protein evolution. Furthermore, we identify a suite of coding genes under positive selection that are putatively associated with pestiferousness in the Colorado potato beetle lineage. They are involved in the biological processes of xenobiotic detoxification, chemosensation and hormone function.

Genome Resequencing Reveals Rapid, Repeated Evolution in the Colorado Potato Beetle

“… a Among these genes, three (the CYP gene LDEC015048, the cuticle protein LDEC010803, and the voltage-dependent calcium channel gene LDEC000112) were found as candidate genes among field populations within Wisconsin ( Crossley et al 2017 ). The nicotinic acetylcholine receptor subunit alpha4 (LDEC007707) was also found as a candidate gene in a comparative genomic analysis of Leptinotarsa by Cohen et al (2021) . …”

“… Schoville et al (2018) found evidence for a high rate of polymorphism in protein-coding regions of CPB (nucleotide diversity, π , was ∼0.01), suggesting a high level of standing genetic diversity and large effective size. Furthermore, CPB shows a larger effective size, higher rate of positive selection, and greater levels of standing variation compared with other species in the genus Leptinotarsa ( Cohen et al 2021 ). In this study, irrespective of pest or nonpest status across different geographical regions, we identify an average genome-wide nucleotide diversity of 0.005 within CPB.…”

“…Although our analysis focuses on pesticide resistance candidates, we note that other interesting genes emerged from our study. In particular, an octopamine receptor (LDEC006841), which was identified as a gene associated with pest behavior in a comparative genomics analysis of CPB ( Cohen et al 2021 ), emerged as a significant target in contrasts of nonpest and pest populations in both LFMM and PCAdapt . The observed patterns of repeated local adaptation are most consistent with evolution from standing genetic variation.…”

Evidence of hard-selective sweeps suggest independent adaptation to insecticides in Colorado potato beetle (Coleoptera:Chrysomelidae) populations

“…From early insecticides such as Paris Green and DDT, to modern insecticides such as pyrethroids and neonicotinoids, CPB populations have accumulated resistance over impressively short periods of time, even within one year (∼2-3 generations) of the introduction of novel chemicals (Forgash 1985, Ioannidis et al 1991, Alyokhin et al 2008; Brevik et al, 2018). In a species-level comparative genomic analysis, CPB shows a higher rate of positive selection on putative insecticide resistant loci compared to other species in the genus Leptinotarsa (Cohen et al . 2020).…”

“…Levels of genome-wide genetic variation are influenced by mutation, recombination, and selection, in direct relationship to effective population size (Hartl and Clark 1997). Prior work suggests that CPB has relatively high genome-wide standing genetic variation (Schoville et al, 2018; Cohen et al, 2020; Pélissié et al, 2022), yet it remains unclear how population history, recombination, and selection interact to shape this variation. Here, we examine the influence of demography and recombination on selection between two highly resistant geographically distinct pest CPB populations in the United States.…”