Consequences of coupled barriers to gene flow for the build-up of genomic differentiation: Reproductive barriers and coupling in corn borers

Authors: KUNERTH, HENRY - Cornell University; BOGDANOWICZ, STEVE - Cornell University; SEARLE, JEREMY - Cornell University; HARRISON, RICHARD - Cornell University; Coates, Brad; KOZAK, GENEVIEVE - University Of Massachusetts; DOPMAN, ERIK - Tufts University

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 9/3/2021
Publication Date: 9/3/2021
Citation: Kunerth, H.D., Bogdanowicz, S.M., Searle, J.B., Harrison, R.G., Coates, B.S., Kozak, G.M., Dopman, E.B. 2021. Consequences of coupled barriers to gene flow for the build-up of genomic differentiation: Reproductive barriers and coupling in corn borers. bioRxiv. Article 458401. https://doi.org/10.1101/2021.09.02.458401.
DOI: https://doi.org/10.1101/2021.09.02.458401

Interpretive Summary: Farmers in the United States manage European corn borer (ECB) damage to maize by planting varieties that express one or more insecticidal Bacillus thuringiensis (Bt) proteins. Recently, detection of Bt resistant ECB populations in Canada has heightened concern for potential spread to the United States. ECB strains can differ in pheromone (mate-attractant) communication systems, in the duration of winter dormancy that results in non-overlapping adult reproductive periods, or both. Differences between strains have an unknown effect in inter-mating and rate at which Bt resistance genes may spread in ECB. An ARS researcher in Ames, Iowa along with university collaborators used prior knowledge that genes controlling duration of dormancy and pheromone communication are located in the same genomic region to determine how these genes interact to form and maintain reproductive barriers in the ECB population. The resulting research determined that ECB populations differing in either duration of dormancy or pheromone communication showed high genetic variation across a relatively narrow area of this genome region. In contrast, when populations that differed in both dormancy and pheromone communication the area of high genetic variation was larger. This work demonstrated that ECB strain differences reduce the rates of gene exchange, but this reduction is only observed in genome regions the encode for genes that control these differences. Genes not in proximity to these gene, such as those for Bt resistance, appear to be unaffected. This research is important for understanding how differences in pest insect populations may impact the spread of Bt resistance genes. This information will be used by regulators, and scientists modeling development and spread of Bt resistance and potential ways to mitigate resistance problems.

Technical Abstract: Theory predicts that when different barriers to gene flow become coincident, their joint effects enhance reproductive isolation and genomic divergence beyond their individual effects, but empirical tests of this ‘coupling’ hypothesis are rare. Here, we analyze patterns of gene exchange among populations of European corn borer moths that vary in the number of acting barriers, allowing for comparisons of genomic variation when barrier traits or loci are in coincident or independent states. We find that divergence is mainly restricted to barrier loci when populations differ by a single barrier, whereas the coincidence of temporal and behavioral barriers is associated with divergence of two chromosomes harboring barrier loci. Furthermore, differentiation at temporal barrier loci increases in the presence of behavioral divergence, while differentiation at behavioral barrier loci increases in the presence of temporal divergence. Our results demonstrate how the joint action of coincident barrier effects leads to levels of genomic differentiation that far exceed those of single barriers acting alone, consistent with theory arguing that coupling allows indirect selection to combine with direct selection and thereby lead to a stronger overall barrier to gene flow. Thus, the state of barriers – independent or coupled – strongly influences the accumulation of genomic differentiation.