Contemporary evolution of a Lepidopteran species, Heliothis virescens, in response to modern agricultural practices

Authors: FRITZ, MEGAN - University Of Maryland; DEYONKE, ALEXANDRA - North Carolina State University; PAPANICOLAOU, ALEXIE - Western Sydney University; MICINSKI, STEPHEN - Louisiana State University; Westbrook, John; GOULD, FRED - North Carolina State University

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/10/2017
Publication Date: 2/2/2018
Citation: Fritz, M.L., Deyonke, A.M., Papanicolaou, A., Micinski, S., Westbrook, J.K., Gould, F. 2018. Contemporary evolution of a Lepidopteran species, Heliothis virescens, in response to modern agricultural practices. Molecular Ecology. 27:167-181.

Interpretive Summary: Tobacco budworm and other pest species may potentially adapt to strong human-induced selection pressure in agricultural ecosystems. Tobacco budworm has been a major insect pest of cotton, yet populations in the southern U.S. have been declining since the widespread planting of transgenic cotton that expresses proteins derived from the bacterium Bacillus thuringiensis (Bt), which are lethal to tobacco budworm. A decline in pyrethroid insecticide use in Bt cotton landscapes likely also led to reversion to pyrethroid susceptibility. Because no physiological adaptation to Bt toxin has been found in tobacco budworm, information is needed to determine if adaptation to this altered environment involves shifts in host plant selection, or changes in detoxification mechanisms required for cotton-feeding. Using novel genetic evaluations, we confirmed a decline in frequency of the pyrethroid-resistance allele (one of two or more alternative forms of a gene that arise by mutation and are found at the same place on a chromosome) in tobacco budworm populations from a 15-year period (1997 to 2012). These genetic evaluations may be useful for identifying resistance alleles, and acting to mitigate widespread pest resistance to management practices across plant and insect species in agricultural ecosystems.

Technical Abstract: Adaptation to human-induced environmental change has the potential to profoundly influence the genomic architecture of affected species. This is particularly true in agricultural ecosystems, where anthropogenic selection pressure is strong. Heliothis virescens feeds on cotton in its larval stages and populations in the Southern United States have been declining since the widespread planting of transgenic cotton. These cotton cultivars endogenously express proteins derived from the bacterium Bacillus thuringiensis (Bt), which are lethal to H. virescens. No physiological adaptation to Bt toxin has been found, so adaptation to this altered environment could involve: 1) shifts in host plant selection mechanisms to avoid cotton, or 2) changes in detoxification mechanisms required for cotton-feeding versus feeding on other host plants. A decline in pyrethroid use in Bt cotton landscapes likely also led to reversion to susceptible alleles at loci involved in expression of pyrethroid resistance. Here we begin to address the question of whether such changes occurred in H. virescens populations between the years 1997 and 2012. In a proof of concept experiment, we confirmed that allele frequency changes at the voltage-gated sodium channel gene, a pyrethroid resistance locus, could be detected through a genomic scanning technique that depends on linkage disequilibrium between molecular markers and gene targets of selection. A direct PCR approach confirmed a decline in frequency of the pyrethroid resistance allele in H. virescens populations over time. We tested the hypothesis that this known genetic change could be detected via a ddRAD-seq enabled genome scan in concert with our new H. virescens genome assembly. Indeed, one ddRAD-seq marker was physically linked to the sodium channel gene, and the rate of allele frequency change at that marker was similar to that of the sodium channel resistance allele. We then identified additional ddRAD-seq loci with significant allele frequency changes over the 15 year study period. Genes near to these ddRAD-seq loci were identified and their potential contributions to adaptive phenotypes in the H. virescens cotton system are discussed.