Selective sweeps in a nutshell; the genomic footprint of rapid insecticide resistance evolution in a major insect pest of tree nuts

Relatively few genome-wide population studies of field-acquired insecticide resistance have been carried out on agricultural pests. Recently acquired bifenthrin resistance in a population of the navel orangeworm (Amyelois transitella), the main insect pest of almond orchards in California, provided an opportunity to examine the short- and long-term effects of heavy insecticide usage in the population genomic landscape of this species. We re-sequenced the genomes of three contemporary A. transitella natural populations differing in bifenthrin resistance status and characterized their population genetics parameters, in the process we detected an exceptionally large selective sweep in all populations. This sweep has virtually no polymorphisms and extends up to 1.3 Mb (spanning 43 genes) in the resistant population. We analyzed the possible causes of this unusually strong population genetic signature, and found genes in the sweep that are associated with DDT and pyrethroid resistance including a cluster of cytochrome P450 coding genes and the gene coding for the small conductance sodium channel "para". Moreover, we found that the sequence along the sweep is nearly identical in the genome assembled from a strain founded in 1966, suggesting that the underpinning for insecticide resistance may have been laid a half-century ago when the California Central Valley experienced massive area-wide applications of DDT for pest control. Our findings are consistent with a scenario whereby insecticide resistance in this species evolved as a stacking of selective pressures that started decades ago and that effectively reduced variation in a region of the genome containing several genes associated with resistance to insecticides with a shared target site and mechanism of action.