Influence of host plant, geography and pheromone strain on genomic differentiation in sympatric populations of Ostrinia nubilalis

Authors: Coates, Brad; KOZAK, GENEVIEVE - Tufts University; KIM, KYUNG SEOK - Iowa State University; SUN, JING - Iowa State University; WANG, YANGZHOU - Jilin Agricultural University; FLEISCHER, SHELBY - Pennsylvania State University; DOPMAN, ERIK - Tufts University; Sappington, Thomas

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/5/2019
Publication Date: 9/8/2019
Citation: Coates, B.S., Kozak, G.M., Kim, K., Sun, J., Wang, Y., Fleischer, S.J., Dopman, E.B., Sappington, T.W. 2019. Influence of host plant, geography and pheromone strain on genomic differentiation in sympatric populations of Ostrinia nubilalis. Molecular Ecology. 28(19):4439-4452. https://doi.org/10.1111/mec.15234.
DOI: https://doi.org/10.1111/mec.15234

Interpretive Summary: The European corn borer (ECB) damages corn in the United States and worldwide. It is a target pest of transgenic corn that express Bacillus thuringiensis (Bt) toxins. Current Environmental Protection Agency insect resistance management (IRM) plans mandate the implementation and use of a high-dose refuge strategy to suppress or circumvent development of Bt resistance in ECB populations. Within this strategy, it is assumed that rare resistant moths that emerge from Bt crops will randomly mate with any of the overwhelming number of susceptible counterparts that emerge from non-Bt refuge plants, reducing the risk of developing resistant populations. ECB populations in the northeast United States are composed of E- and Z-strains that differ in the pheromone blend used by females to attract males. The two strains are also reported to show different host plant preferences, which could reduce random mating and thereby impact the efficacy of IRM strategies. Use of DNA markers demonstrated that E- and Z-strain ECB populations were surprisingly similar. Nevertheless, male pheromone response traits and female pheromone production traits accounted for most of the differences that did exist. In contrast, differences in host plants used by larvae was not a significant factor that influenced genetic differentiation between ECB populations. These data indicate that genes physically located in the genome near the genes determining pheromone strain may impact random mating and the efficacy of IRM strategies. These data are of interest to university, industry, and regulatory stakeholders involved in the management of pest insect resistance to Bt crops.

Technical Abstract: E- and Z-strains of the European corn borer, Ostrinia nubilalis, are sympatric in the northeast United States, wherein females produce and males preferentially respond to 97:3 and 1:99 pheromone blends of E- or Z-delta11-tetradecenyl acetate (E11- and Z11-14:OAc), respectively. Divergent selection at the pheromone gland fatty acyl-reductase (pgfar) locus determines stereoisomeric ratio differences of female pheromone blends, and strains may differ in preference for host plants in C3 or C4 photosynthetic pathway. Genetic differentiation was estimated between sympatric male O. nubilalis collected using E11- and Z11-14:OAc lure-bated traps at 12 locations in Pennsylvania and New York between 2007 and 2010. Principal coordinate, Bayesian clustering, and distance-based redundancy analysis (dbRDA) demonstrate that C3 or C4 host plant history does not significantly contribute to population variation or differentiation between males partitioned by pgfar genotype or pheromone lure to which males are attracted. In contrast, geographic distance, pheromone lure, and pgfar-defined strain contribute significantly to O. nubilalis population genetic differentiation. Despite linkage to differences in female produced pheromone blend, the pgfar locus accounts for approximately 64% of the variance between males partitioned by pheromone lure, suggesting a degree of concerted evolution with unlinked loci controlling reproductive traits. Furthermore, directional sexual selection at pgfar influenced Bayesian clustering analyses despite partitioning genotypes by lure and host plant. This study implicates divergence based on male pheromone attraction and pheromone strain (sexual selection), as opposed to ecological selection base on host plant utilization, as important components involved in the maintenance of variation in sympatric O. nubilalis populations.