Dual domestication, diversity, and differential introgression in Old World cotton diploids

Authors: GROVER, CORRINNE - Iowa State University; ARICK II, MARK - Mississippi State University; THRASH, ADAM - Mississippi State University; SHARBROUGH, JOEL - New Mexico Institute Of Mining & Technology; HU, GUANJING - Chinese Academy Of Agricultural Sciences; YUAN, DAOJUN - Huazhong Agricultural University; MILLER, EMMA - Iowa State University; RAMARAJ, THIRUVARANGAN - Depaul University; PETERSON, DANIEL - Mississippi State University; Udall, Joshua - Josh; WENDELL, JONATHAN - Iowa State University

Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/1/2022
Publication Date: 12/13/2022
Citation: Grover, C.E., Arick II, M.A., Thrash, A., Sharbrough, J., Hu, G., Yuan, D., Miller, E.R., Ramaraj, T., Peterson, D.G., Udall, J.A., Wendell, J.F. 2022. Dual domestication, diversity, and differential introgression in Old World cotton diploids. Genome Biology and Evolution. 14(12). https://doi.org/10.1093/gbe/evac170.
DOI: https://doi.org/10.1093/gbe/evac170

Interpretive Summary: This work describes the genetic diversity of the domesticated cotton species Gossypium herbaceum. G. herbaceum is from Asia/Africa and it's genetic history and has not been previously studied using whole-genome sequencing methods. This study clearly demonstrates that G. herbaceum evolved independently from G. arboreum, despite previous claims to the contrary.

Technical Abstract: Domestication in the cotton genus is remarkable in that it has occurred independently four different times at two different ploidy levels. Relatively little is known about genome evolution and domestication in the cultivated diploid species Gossypium herbaceum and G. arboreum, because of the absence of wild representatives for the latter species, their ancient domestication, and their joint history of human-mediated dispersal and interspecific gene flow. Using in-depth resequencing of a broad sampling from both species, we confirm their independent domestication, as opposed to a progenitor-derivative relationship, showing that diversity (mean pi = 2.3×10-3) within species is similar, and that divergence between species is modest (weighted FST=0.4430). Individual accessions were homozygous for ancestral SNPs at over half of variable sites, while fixed, derived sites were at modest frequencies. Notably, two chromosomes with a paucity of fixed, derived sites (i.e., chromosomes 7 and 10) were also strongly implicated in introgression analyses. Collectively, these data demonstrate variable permeability to introgression among chromosomes, which we propose is due to divergent selection under domestication and/or the phenomenon of F2 breakdown in interspecific crosses. Our analyses provide insight into the evolutionary forces influencing diversity and divergence in the diploid cultivated species, and establish a foundation for understanding the contribution of introgression and/or strong parallel selection to the extensive morphological similarities shared between species.