Parallel and Intertwining Threads of Domestication in Allopolyploid Cotton

Abstract

The two cultivated allopolyploid cottons, Gossypium hirsutum and Gossypium barbadense, represent a remarkable example of parallel independent domestication, both involving dramatic morphological transformations under selection from wild perennial plants to annualized row crops. Deep resequencing of 643 newly sampled accessions spanning the wild-to-domesticated continuum of both species, and their allopolyploid relatives, are combined with existing data to resolve species relationships and elucidate multiple aspects of their parallel domestication. It is confirmed that wild G. hirsutum and G. barbadense were initially domesticated in the Yucatan Peninsula and NW South America, respectively, and subsequently spread under domestication over 4000-8000 years to encompass most of the American tropics. A robust phylogenomic analysis of infraspecific relationships in each species is presented, quantify genetic diversity in both, and describe genetic bottlenecks associated with domestication and subsequent diffusion. As these species became sympatric over the last several millennia, pervasive genome-wide bidirectional introgression occurred, often with striking asymmetries involving the two co-resident genomes of these allopolyploids. Diversity scans revealed genomic regions and genes unknowingly targeted during domestication and additional subgenomic asymmetries. These analyses provide a comprehensive depiction of the origin, divergence, and adaptation of cotton, and serve as a rich resource for cotton improvement.

Comparative genomics and polyploid dynamics in tetraploid cotton (Gossypium)

“…We observed similar divergence times between Gb-Gd (0.63 Mya; 95% CI: 0.37-1.26 Mya) and GhP-Gh (0.68 Mya; 95% CI: 0.41-1.14 Ma), con rming earlier data indicating that the Galapagos Island endemic G. darwinii (Gd), previously considered to be conspeci c with G. barbadense, diverged relatively recently from its mainland relative [40]. The genome sequences for the two species Ge and Gs complete the sampling of wild tetraploid Gossypium, and, as expected from prior analyses [10][11][12], they fall within the Gh-like clade, having all diverged from their most recent common ancestor around 0.75 Mya (95% CI, 0.42 -1.33 Mya) (Supplementary Fig. 5).…”

“…Remarkably, an inversion event larger than 986.42 Kb on D01 was observed in both domesticated Gb and Gh (Fig. 3c), suggesting either a remarkable convergence under human selection, or more likely introgression between the two species, which has been common [12].…”

“…This new allopolyploid clade subsequently diversi ed into the seven species recognized today (AD 1 -AD 7 ) [8,9]. Tetraploid cottons provide an important model system for understanding evolutionary consequences of polyploids, as well as dual domestication [10][11][12]. Among the seven species of allopolyploid Gossypium, two, i.e., Gh (G. hirsutum, genome designation AD 1 ) and Gb (G. barbadense, genome designation AD 2 ), provide the majority of natural ber for commercial production [13,14].…”

Deleterious Mutations Accumulate Faster in Allopolyploid than Diploid Cotton (Gossypium) and Unequally Between Subgenomes

“…We found that the At subgenome of all species contains 2-3% more nonsynonymous mutations that are inferred to be deleterious (Figure 3) even when only considering mutations that have arisen following the earliest allopolyploid diversification events, and correcting for removing the biases of unequal phylogenetic distances to each subgenome’s model progenitor diploid. Our work adds to a growing recognition that the two co-resident subgenomes in cotton allopolyploids may be shaped asymmetrically by evolutionary processes, including interspecific introgression and selection under domestication (Fang, Wang, et al 2017; Fang, Guan, et al 2017; Chen et al 2020; Yuan et al 2021), and that this phenomenon also extends to other important allopolyploid crop plants, including wheat (Pont and Salse 2017; Jiao et al 2018) and Brassica (Tong et al 2020) .…”

“…Included in our sampling was six polyploid species originating from a single polyploidization event 1-2 million years ago (Wendel 1989; Hu et al 2021), two diploid species representing models of the genome donors to the allopolyploids (A and D), and three species from Australia that served as outgroups for polarizing SNPs into ancestral and derived states. These sequences were previously described (Yuan et al 2021), and SRA codes for all 46 resequenced individuals are listed in Supplemental Table 1. For G. hirsutum , we randomly chose ten accessions that were classified in the “Wild” population from Yuan et al (Yuan et al 2021), and for the other species, we chose all accessions available that did not show evidence of being mislabeled, as determined by a PCA plot of the SNPs called.…”