Despite their economic importance and well-characterized domestication syndrome, the genomic impact of domestication and the identification of variants underlying the domestication traits in Cucurbita species (pumpkins and squashes) is currently lacking. Cucurbita argyrosperma, also known as cushaw pumpkin or silver-seed gourd, is a Mexican crop consumed primarily for its seeds rather than fruit flesh. This makes it a good model to study Cucurbita domestication, as seeds were an essential component of early Mesoamerican diet and likely the first targets of human-guided selection in pumpkins and squashes. We obtained population-level data using tunable Genotype by Sequencing libraries for 192 individuals of the wild and domesticated subspecies of C. argyrosperma across Mexico. We also assembled the first high-quality wild Cucurbita genome. Comparative genomic analyses revealed several structural variants and presence/absence of genes related to domestication. Our results indicate a monophyletic origin of this domesticated crop in the lowlands of Jalisco. We found evidence of gene flow between the domesticated and wild subspecies, which likely alleviated the effects of the domestication bottleneck. We uncovered candidate domestication genes that are involved in the regulation of growth hormones, plant defense mechanisms, seed development, and germination. The presence of shared selected alleles with the closely related species Cucurbita moschata suggests domestication-related introgression between both taxa.

Analyses of genetic variation allow understanding the origin, diversification and genetic resources of cultivated plants. Domesticated taxa and their wild relatives are ideal systems for studying genetic processes of plant domestication and their joint is important to evaluate the distribution of their genetic resources. Such is the case of the domesticated subspecies C. argyrosperma ssp. argyrosperma, known in Mexico as calabaza pipiana, and its wild relative C. argyrosperma ssp. sororia. The main aim of this study was to use molecular data (microsatellites) to assess the levels of genetic variation and genetic differentiation within and among populations of domesticated argyrosperma across its distribution in Mexico in comparison to its wild relative, sororia, and to identify environmental suitability in previously proposed centers of domestication. We analyzed nine unlinked nuclear microsatellite loci to assess levels of diversity and distribution of genetic variation within and among populations in 440 individuals from 19 populations of cultivated landraces of argyrosperma and from six wild populations of sororia, in order to conduct a first systematic analysis of their genetic resources. We also used species distribution models (SDMs) for sororia to identify changes in this wild subspecies’ distribution from the Holocene (∼6,000 years ago) to the present, and to assess the presence of suitable environmental conditions in previously proposed domestication sites. Genetic variation was similar among subspecies (H_E = 0.428 in sororia, and H_E = 0.410 in argyrosperma). Nine argyrosperma populations showed significant levels of inbreeding. Both subspecies are well differentiated, and genetic differentiation (F_ST) among populations within each subspecies ranged from 0.152 to 0.652. Within argyrosperma we found three genetic groups (Northern Mexico, Yucatan Peninsula, including Michoacan and Veracruz, and Pacific coast plus Durango). We detected low levels of gene flow among populations at a regional scale (<0.01), except for the Yucatan Peninsula, and the northern portion of the Pacific Coast. Our analyses suggested that the Isthmus of Tehuantepec is an effective barrier isolating southern populations. Our SDM results indicate that environmental characteristics in the Balsas-Jalisco region, a potential center of domestication, were suitable for the presence of sororia during the Holocene.

Cucurbita pepois an economically important crop, which consists of cultivatedC. pepossp.pepo, and two wild taxa (C. pepossp.fraternaandC. pepossp.ovifera).We aimed at understanding the domestication and the diversity ofC. pepoin Mexico. We used two chloroplast regions and nine nuclear microsatellite loci to assess the levels of genetic variation and structure forC. pepossp.pepo's landraces sampled in 13 locations in Mexico, five improved varieties, oneC. pepossp.fraternapopulation and ornamentalC. pepossp.ovifera. We tested four hypotheses regarding the origin ofC. pepossp.pepo's ancestor through approximate Bayesian computation:C. pepossp.oviferaas the ancestor;C. pepossp.fraternaas the ancestor; an unknown extinct lineage as the ancestor; andC. pepossp.pepoas hybrid fromC. pepossp.oviferaandC. pepossp.fraternaancestors.Cucurbita pepossp.peposhowed high genetic variation and low genetic differentiation.Cucurbita pepossp.fraternaandC. pepossp.peposhared two chloroplast haplotypes. The three subspecies were well differentiated for microsatellite loci.Cucurbita pepossp.fraternawas probablyC. pepossp.pepo's wild ancestor, but subsequent hybridization between taxa complicate definingC. pepossp.pepo's ancestor.