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 and 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.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
The authors declare that there are no conflicts of interest pertaining to this study.
All data is archived in GenBank: PRJNA361472 ; PRJNA540655 ; PRJNA655940 ; PRJNA656263 ; PRJNA794858
Text was edited throughout to reduce total word count. One paragraph in the conclusions section was removed, as it was part of an extended discussion and we wanted to reduce total word count for submission to a journal. Figure 7 was moved to the supplementary files and replaced with a similar figure that focuses on the entire chromosomal pattern, rather than subdivisions between collinear and rearranged regions. Typo corrected on line 164. January 2022 changes below Updated the cover page and author list to correct and authors name and added a conflict of interest statement. Corrected various typos throughout the paper and added citations throughout. Adjusted figure 1 for an error. Added version numbers to software. Moved some text from results to methods. Corrected minor error in figure 2. Updated some p-values following revisions. No interpretations changed. Added a missing significance bar in figure 3. Changed clarity of figure 5.