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

Abstract

19Insect pests are characterized by expansion, preference and performance on agricultural 20 crops, high fecundity and rapid adaptation to control methods, which we collectively refer to as 21 pestiferousness. Which organismal traits and evolutionary processes facilitate certain taxa 22 becoming pests remains an outstanding question for evolutionary biologists. In order to 23 understand these features, we set out to test the relative importance of genomic properties that 24 underlie the rapid evolution of pestiferousness in the emerging pest model: the Colorado potato 25 beetle (CPB), Leptinotarsa decemlineata Say. Within the Leptinotarsa genus, only CPB has 26 risen to pest status on cultivated Solanum. Using whole genomes from ten closely related 27 Leptinotarsa species, we reconstructed a high-quality species tree of this genus. Within this 28 phylogenetic framework, we tested the relative importance of four drivers of rapid adaptation: 29 standing genetic variation, gene family expansion and contraction, transposable element 30 variation, and protein evolution. Throughout approximately 20 million years of divergence, 31 Leptinotarsa show little evidence of gene family turnover or transposable element variation 32 contributing to pest evolution. However, there is a clear pattern of pest lineages experiencing 33 greater rates of positive selection on protein coding genes, as well as retaining higher levels of 34 standing genetic variation. We also identify a suite of positively selected genes unique to the 35 Colorado potato beetle that are directly associated with pestiferousness. These genes are 36 involved in xenobiotic detoxification, chemosensation, and hormones linked with pest behavior 37 and physiology.38 39

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

“…Unlike other major agricultural pest species, CPB experienced a host expansion onto potato and switched to pest status in part of its endemic range, North America (eastern Nebraska) in 1859 (Walsh 1866). The host expansion of CPB allowed for the retention of high standing genetic diversity as the pest extended its range eastward (Cohen et al 2020;Pélissié et al, 2022;Izzo et al, 2018). Geographical structure was shown in earlier population genetic studies using microsatellites, AFLPs, and mitochondrial DNA (Grapputo et al, 2005;Izzo et al, 2018).…”

“…Genes in these protein families have been linked with pesticide detoxification in CPB and other insect pests (Jao and Casida 1974;Bhatt et al, 2020;Cohen et al, 2020;Crossley et al, 2019;Lü et al, 2015). The Long Island population is one of the most abundant and insecticide resistant CPB populations in the literature (Alyokhin et al 2015;Dively et al, 2020).…”

“…Until recently, most research on CPB focused on well-known target genes and metabolic pathways (Alyokhin et al 2008). As next generation sequencing technology and genomic resources have become available for CPB (Kumar et al, 2014;Cohen et al, 2020), there has been a rapid expansion of knowledge into the genetic basis of pesticide resistance using genome scans as an agnostic approach to gene discovery. With respect to prior comparative population genetic studies of CPB, which had presented extensive candidate gene lists (>8,700 genes from a more inclusive demographic sampling; Pélissié et al, 2022), this work suggests a small set of genes (<150 per population) undergo hard selective sweeps.…”

“…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 2008Brevik 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). Recent population genomic sequencing studies of CPB have found evidence for selection acting on many insecticide resistance pathways, supporting a prominent role of polygenic adaptation to insecticides over time (Crossley et al, 2017;Pélissié et al, 2022).…”

“…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 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.…”