ddRAD Sequencing Identifies Pesticide Resistance-Related Loci and Reveals New Insights into Genetic Structure of Bactericera cockerelli as a Plant Pathogen Vector

SIMPLE SUMMARY: Insect vectors of plant diseases and insecticide resistance pose the greatest challenge to sustainable crop production in food security. In this study, we explored genetic mechanisms responsible for resistance to a common insecticide group, neonicotinoids, in a key insect vector of potato diseases—potato psyllids. These small insects with piercing-sucking mouthparts are common in potato and can transmit a bacterium that causes zebra chip disease. Zebra chip has had a devastating impact on potato producers and has contributed to a highly regimented and intense use of insecticides to suppress potato psyllids as soon as they are detected in a field, commonly using neonicotinoids. Widespread resistance to these insecticides is now evident in potato psyllid populations. Using susceptible and resistant psyllid populations, we sequenced portions of their genomes to elucidate genes involved in the evolution of resistance to neonicotinoid insecticides. We found several genes that are likely to be responsible for insecticide resistance, and these should be explored in further research. We also discovered that a method commonly used to separate potato psyllids into distinct groups based on their geographic origin does not adequately represent their genetic population structure and should be used in conjunction with other genetic techniques. ABSTRACT: (1) Background: Many hemipteran insects transmit plant pathogens that cause devastating crop diseases, while pest management frequently relies primarily on insecticide applications. These intense insecticide applications lead to the development of insecticide resistance, as was the case for potato psyllid, Bactericera cockerelli (Hemiptera: Triozidae), a vector of Candidatus Liberibacter solanacearum, which causes zebra chip disease in potato. (2) Methods: Here, we use double-digest restriction site-associated DNA (ddRAD) to genotype eight psyllid populations (one susceptible and seven resistant to neonicotinoid insecticides). (3) Results: Association tests identified over 400 loci that were strongly segregated between susceptible and resistant populations. Several loci were located within genes involved in insecticide resistance, gene regulation, fertility, and development. Moreover, we explored the genetic structure of these eight populations and discovered that routinely utilized haplotyping was not an accurate predictor of population structure. Pairwise comparisons of the fixation index (F(ST)) of populations of the same haplotype were not different from pairwise F(ST) of populations that belonged to different haplotypes. (4) Conclusions: Our findings suggest that neonicotinoid insecticide resistance has a genetic basis, most likely as a result of similar selection pressure. Furthermore, our results imply that using a single maternally inherited gene marker to designate genetic lineages for potato psyllids should be re-evaluated.