Selective sweeps in a nutshell: the genomic footprint of rapid insecticide resistance evolution in the almond agroecosystem

Authors: CALLA, BERNARDA - University Of Illinois; DEMKOVICH, MARK - University Of Illinois; GOMES-VIANA, JOAO - University Of Illinois; Siegel, Joel; WALDEN, KIM - University Of Illinois; ROBERTSON, HUGH - University Of Illinois; BERENBAUM, MAY - University Of Illinois

Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/1/2020
Publication Date: 11/4/2020
Citation: Calla, B., Demkovich, M.R., Gomes-Viana, J.P., Siegel, J.P., Walden, K.K., Robertson, H.M., Berenbaum, M.R. 2020. Selective sweeps in a nutshell: the genomic footprint of rapid insecticide resistance evolution in the almond agroecosystem. Genome Biology and Evolution. 13(1). https://doi.org/10.1093/gbe/evaa234.
DOI: https://doi.org/10.1093/gbe/evaa234

Interpretive Summary: The navel orangeworm, Amyelois transitella, is the principal insect pest of almonds and pistachios (>1.5 million acres) grown in California, valued at >$7 billion in 2018. Insecticides currently play a major role in controlling this moth, but because of their extensive use development of insecticide resistance is a major concern. In 2013, 10-fold resistance to the pyrethroid insecticide bifenthrin was reported and a colony of resistant moths was established. The genes associated with insecticide detoxification were examined in this colony as well as other colonies established from almonds and figs, with the goal of comparing the variability of resistant and susceptible populations of navel orangeworm, looking for “a selective sweep”. A selective sweep occurs when a rare gene increases the fitness of the carrier; in this case the ability to detoxify pyrethroid insecticides, drastically reducing genetic variation in the population, including variation in adjacent genes. A large selective sweep occurred in the resistant colony, spanning 43 genes. This is the largest described from an insect, and a similar but smaller selective sweep (22 genes) was also present in the colonies originating from collections made in almonds and figs over the past five years. All of these colonies contained a mutation “kdr” associated with both pyrethroid and DDT resistance, which would be consistent with previous heavy exposure to DDT. Individuals from a susceptible colony established in 1966 did not have the kdr genetic mutation but had other genes in this sweep region responsible for increased detoxification activity, providing further evidence of heavy exposure to DDT. Possession of the kdr mutation gave 10-fold resistance to both pyrethroids and DDT compared to the baseline susceptible colony. The results support the hypothesis that the navel orangeworm was preadapted for pyrethroid resistance because of previous exposure to DDT as well as mutations in detoxification genes belonging to the cytochrome P450 family.

Technical Abstract: The size of selective sweeps -reductions in nucleotide diversity in genome regions flanking genes under positive selection--depends on the strength and timing of the underlying selective pressure. The navel orangeworm Amyelois transitella is a pest of nut and fruit crops that has been subjected to extensive pyrethroid insecticide applications in California’s Central Valley. Recently, resistance to bifenthrin, a pyrethroid, arose in almond orchards in Kern County. We re-sequenced the genomes of three contemporary A. transitella natural populations differing in resistance status and detected an exceptionally large selective sweep present in all populations, and with virtually no polymorphisms across 0.6 Mb (spanning 22 genes), with the sweep in the pyrethroid resistant line extending even longer (1.3 Mb total), spanning 43 genes. At the leftmost position of the hard sweep in all lines is the para gene carrying the kdr mutation, long associated with DDT and pyrethroid resistance and in the approximate center of the sweep is a cluster of three cytochrome P450 genes from sub-families associated with pyrethroid resistance in other insects. A review of past pesticide use in almonds in the Central Valley indicates that this genomic signature could have emerged in under five years, during which time patent expiration and product diversification were associated with increases in total pounds of bifenthrin applied increased up to 7-fold. Moreover, the nucleotide sequence along the hard-sweep region is nearly identical to that the reference genome across coding regions. The reference was assembled from a strain founded in 1966, suggesting that the foundation for the rapid appearance of bifenthrin resistance may have been laid a half-century ago when the Central Valley experienced massive use of aerially applied DDT. Our findings illustrate the impact of human-induced selective pressure on insect genomes and the long-term evolutionary consequences of short-term economically driven management decisions.