Pangenomics Links Boll Weevil Divergence With Ancient Mesoamerican Cotton Cultivation

The boll weevil, Anthonomus grandis grandis Boheman, and thurberia weevil, Anthonomus grandis thurberiae Pierce, together comprise a species complex that ranges throughout Mexico, the southwestern regions of the United States and parts of South America. The boll weevil is a historically damaging and contemporaneously threatening pest to commercial upland cotton, Gossypium hirsutum L. (Malvales: Malvaceae), whereas the thurberia weevil is regarded as an innocuous non-pest subspecies that is mostly found on non-cultivated Thurber's or Arizona cotton, Gossypium thurberi L., throughout its native range in western Mexico and the southwestern United States. Recent independent analyses, using mitochondrial and whole-genome markers, have suggested the independent evolution of these lineages is more attributable to geographic isolation than biotic factors. We suggest a combination of drivers after employing comparative genomic, population genetic and pangenome methodologies to identify large and small polymorphisms. By leveraging genetic differences, we determined 39,310 diagnostic loci between the subspecies, find genes under selection, and model the subspecies' shared and unique evolutionary history. Interestingly, structural variations capture a large proportion of genes at the population level and demographic reconstruction suggests a split between approximately 3,320-16,300 before present (YBP), which coincides with cotton cultivation in Mesoamerica, approximately 3,000-5,000 YBP. Observed polymorphisms are enriched for reproductive, regulatory, and metabolic genes, which may be attributed to the subspecies split and coevolution with cultivated cotton. Our results demonstrate the utility of a holistic, comparative framework utilising small and large polymorphisms to reconstruct demography and identify genetic novelty via pangenomics.