High levels of genetic variation and differentiation in wild tropical gourds provide a novel resource for cucurbit crop improvement

Abstract

The genetic variation of crop wild relatives will be key for our survival, as environmental change represents an increasing global threat for agriculture and food security. Cucurbita lundelliana and Cucurbita okeechobeensis subsp. martinezii are wild relatives of cultivated squashes and pumpkins that could be used for crop improvement. A genomic approach was used to characterize genetic resources in these taxa, that is, to identify candidate sites in the genome involved in responses to abiotic stress, and to understand the roles of gene flow and environmental differentiation in their divergence. This study highlights the importance of conserving these two species as phytogenetic resources for crop improvement. Crop wild relatives (CWR) are reservoirs of genetic diversity and they are important for the maintenance of crop evolutionary potential. Mexico is the centre of domestication and diversity for many CWR. The genus Cucurbita originated in America, where at least six independent domestication events took place. Nonetheless, Cucurbita CWR have been seldom studied. In the present study, we test the role of incomplete lineage sorting (ILS) and secondary contact in the divergence of C. okeechobeensis subsp. martinezii and C. lundelliana. Additionally, we seek to understand the role of environmental differentiation in their divergence. We obtained 1,638 single nucleotide polymorphisms (SNPs) for 107 individuals from the most recently diverged wild species in this genus, encompassing 25 localities of C. lundelliana and nine localities of C. okeechobeensis subsp. martinezii in Mexico. We found higher genetic variation in C. lundelliana (HE = 0.227) than in C. okeechobeensis subsp. martinezii (HE = 0.187). Each taxon constitutes a well‐differentiated genetic group, with an area of introgression in Pantanos de Centla. We found candidate loci associated to hydric and thermal stress, which could be valuable for crop improvement. Our study supported a scenario of ILS followed by secondary contact, where divergence was probably driven by Pleistocene climate change. These CWR represent important phytogenetic resources for crop improvement given their high levels of genetic variation and differentiation and their SNPs associated to different climatic variables.