Consequences of coupled barriers to gene flow for the build-up of genomic differentiation

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: Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/29/2021
Publication Date: 3/19/2022
Citation: Kunerth, H.D., Bogdanowicz, S.M., Searle, J.B., Harrison, R.G., Coates, B.S., Kozak, G.M., Dopman, E.B. 2022. Consequences of coupled barriers to gene flow for the build-up of genomic differentiation. Evolution. 76(5):985-1002. https://doi.org/10.1111/evo.14466.
DOI: https://doi.org/10.1111/evo.14466

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, the level of variation in this genome region increased when populations that differed in both dormancy and pheromone communication were compared. 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 genes, 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: Speciation proceeds by reducing the possibility of gene flow between populations. Thus, it is facilitated by accumulation of barrier loci encoding traits which restrict such genetic exchange. In this study, we explore gene exchange in European corn borer moths, Ostrinia nubilalis Hübner, between populations that differ in numbers of barriers. We contrast the action of a single barrier to gene exchange (voltinism or pheromone signaling) acting separately with that of these same barriers acting concurrently, occurring in coincidence and explore their effects on levels of chromosome divergence at non-barrier loci. Here, we utilize two datasets to assess divergence at key loci and across the genome. We utilize a targeted approach of amplicon markers across the length of the Z chromosome, a sex chromosome in the ZW/ZZ system, as it contains key loci controlling barrier phenotypes in corn borers and contains a large region of recombination suppression. We also analyze a pooled sequencing dataset to assess levels of divergence at all chromosomes. We show that divergence is restricted to a rearranged region on the Z chromosome when interbreeding populations differ by a single barrier gene, while the presence of two coupled barriers to gene exchange facilitates greater chromosomal divergence at Z chromosome-linked loci. Further, we demonstrate that the combined effect of coupled barriers facilitates indirect selection at barrier loci and across the Z-chromosome. These combined effects (elevated allelic divergence and linkage disequilibrium between key barrier loci) provide a mechanism for the establishment of new species.