Evolution of the Cotton Genus, Gossypium, and Its Domestication in the Americas

Abstract Gossypium, the cotton genus, includes ∼50 species distributed in tropical and sub-tropical regions of all continents except Europe. Here we provide a synopsis of the evolutionary history of Gossypium and domestication of the American allopolyploid species, integrating data from fundamental taxonomic investigations, biogeography, molecular genetics, phylogenetic analysis, and archaeology. These diverse sources of information provide a temporal and phylogenetic perspective on diversification among the diploids and on polyploid formation, uncover multiple previously cryptic interspecific hybridizations, clarify and contribute to the taxonomy of the genus, and offer a firm foundation for understanding parallel domestications in Mesoamerica and South America, which led to the globally important cotton crop species G. barbadense and G. hirsutum. Gossypium thus offers a testimonial example of the importance and utility of fundamental botanical discovery combined with modern technological capabilities to generate genomic insights into evolutionary history. We also review the current state of our knowledge regarding the archaeological history of cotton domestication and diffusion in the Americas, a seemingly unlikely story entailing parallel domestication origins and parallel directional selection tracing to 8,000 (G. barbadense) and 5,500 (G. hirsutum) years ago, transforming two geographically isolated wild short-day perennial shrubs having small capsules and seeds covered by short, tan-colored epidermal trichomes into modern daylength-neutral annuals bearing abundant, fine, strong white fibers. This dual domestication was followed several millennia later by unintentional and more recently intentional interspecific introgression, as the two species came into contact following their initial domestication in different hemispheres. Thus, the cycle of species divergence and biological reunion was reiterated, this time at the allopolyploid level. Understanding this evolutionary history is vitally important to our understanding of the genomic architecture of the world’s most important fiber plant and contributes substantially to our understanding of general biological principles.