The domestication of Cucurbita argyrosperma as revealed by the genome of its wild relative

Abstract

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.

Targeted Sequencing Suggests Wild-Crop Gene Flow Is Central to Different Genetic Consequences of Two Independent Pumpkin Domestications

“…sororia on the Pacific coast that share more alleles with the domesticate may represent a more specific geographic origin for the initial domestication of cushaw in Mexico. This result is congruent with recent findings by Sánchezde la Vega et al (2018) and in particular Barrera-Redondo et al (2021) that used coalescent models of domestication and genetic differentiation tests (F ST ) to show that C. argyrosperma ssp. sororia populations from Jalisco, Mexico, are most closely related to domesticated C. argyrosperma ssp.…”

Recent and Historical Gene Flow in Cultivars, Landraces, and a Wild Taxon of Cucurbita pepo in Mexico

“…The latter may relate to C. pepo being the pumpkin species with higher commercial importance and higher morphological diversity (Paris, 2001). Accordingly, we expect cultivated C. pepo to show high effective population sizes, and high dispersal through anthropogenic movements, which is further supported by a lack of genetic structure, in contrast to C. argyrosperma and C. moschata in Mexico (Sánchez-de la Vega et al, 2018;Castellanos-Morales et al, 2019;Hernández-Rosales et al, 2020;Barrera-Redondo et al, 2021). In our analyses, the ornamental mix (C. pepo ssp.…”

“…argyrosperma) and its wild relative (C. argyrosperma ssp. sororia), Barrera-Redondo et al (2021) found that many derived sites are shared between taxa-that is, they found an "AABB" pattern -. The latter means that lineages in C. argyrosperma are well differentiated (monophyletic).…”

“…Also, for C. argyrosperma there was genomic evidence of extant gene flow after initial domestication (Barrera-Redondo et al, 2021). The observed differences between C. pepo and C. argyrosperma may relate to differences in their domestication history-reticulate domestication followed by rapid expansion in C. pepo vs. single domestication followed by gene flow in C. argyrosperma (Andres, 1987;Castellanos-Morales et al, 2019;Barrera-Redondo et al, 2021) -. Also, trade and management patterns differ between these species, as C. argyrosperma ssp.…”

“…Also, trade and management patterns differ between these species, as C. argyrosperma ssp. argyrosperma is traded mainly at a local level and there are well defined genetic clusters in this taxon (Sánchez-de la Vega et al, 2018;Barrera-Redondo et al, 2021), while trade for C. pepo ssp. pepo occurs at a larger scale (Lira, 1995;Zizumbo and Colunga, 2008;Mera Ovando et al, 2011).…”