Graph-based pangenome provides insights into the adaptive evolution of Cucurbita pepo

Abstract

Understanding how crops respond to environmental variation is crucial for biodiversity conservation and food security. Cucurbita pepo (pumpkin, squash, gourd) is one of the first domesticated crop species and exhibits remarkable phenotypic and ecological diversity, making it a powerful system for investigating the genomic basis of adaptation. Here, we constructed a graph-based C. pepo pangenome using nine chromosome-level assemblies and identified 229,431 high-confidence structural variants (SVs) that were genotyped across 206 wild and cultivated accessions. Our results demonstrate that C. pepo underwent parallel domestication, with two deeply diverged gene pools independently giving rise to the pepo and ovifera cultivated lineages, followed by expansion into diverse environments that produced strong signatures of differentiation largely mediated by young adaptive alleles. Single-nucleotide polymorphisms (SNPs) and SVs contribute complementary dimensions of environmental responsiveness. Biogeographical modeling predicts continued range contraction of wild relatives and elevated genetic offset in Eastern North American populations under projected future climates. Populations with higher genetic load harbor fewer adaptive variants and exhibit greater predicted maladaptation, indicating that deleterious mutations constrain adaptive potential. These findings highlight how genomic variants, adaptive diversity, and genetic load together shape environmental adaptation and inform conservation and crop improvement.