Pangenomics Links Boll Weevil Divergence with U.S. Cotton Cultivation
Abstract
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The boll weevil, Anthonomus grandis grandis Boheman, and thurberia
weevil, Anthonomus grandis thurberiae Pierce (Coleoptera:
Curculionidae), together comprise a species complex that ranges
throughout Mexico, the southwestern regions of the United States, and
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 Gossypium species, e.g. Thurber’s or Arizona
cotton, G. thurberi, throughout its native range in western parts of
Mexico and the southwestern US. Recent independent analyses using
mitochondrial COI and whole genome ddRADseq have suggested the
independent evolution of these lineages is largely attributable to
geographic isolation and not to host plant preference. We furthered this
investigation by employing comparative genomic, population genetic, and
pangenome methodologies to identify large and small polymorphisms within
this complex and described their role in demography and adaptation. We
also leveraged genetic differences to identify nearly 40,000 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
these subspecies that coincides with cotton cultivation in the southern
U.S. in the late 1800s. Observed polymorphisms are enriched for
reproductive, regulatory, and metabolic genes which may be attributed to
the boll weevil’s rapid expansion onto commercial cotton.