Gourds and squashes (Cucurbitaspp.) adapted to megafaunal extinction and ecological anachronism through domestication

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-12, Vol.112 (49), p.15107-15112
• Main Authors: Kistler, Logan, Newsom, Lee A., Ryan, Timothy M., Clarke, Andrew C., Smith, Bruce D., Perry, George H.
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological; Biological Sciences; Cucurbita; Cucurbita - genetics; Cucurbita - physiology; Dispersal; Ecology; Extinction; Extinction, Biological; Genes; Genome, Plant; Genomes; Herbivores; Mammals; Molecular Sequence Data; Plastids; Plastids - genetics; Social Sciences; Symbiosis; Vegetables
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1516109112

The genusCucurbita(squashes, pumpkins, gourds) contains numerous domesticated lineages with ancient New World origins. It was broadly distributed in the past but has declined to the point that several of the crops’ progenitor species are scarce or unknown in the wild. We hypothesize that Holocene ecological shifts and megafaunal extinctions severely impacted wildCucurbita,whereas their domestic counterparts adapted to changing conditions via symbiosis with human cultivators. First, we used high-throughput sequencing to analyze complete plastid genomes of 91 totalCucurbitasamples, comprising ancient (n= 19), modern wild (n= 30), andmodern domestic (n= 42) taxa. This analysis demonstrates independent domestication in eastern North America, evidence of a previously unknown pathway to domestication in northeastern Mexico, and broad archaeological distributions of taxa currently unknown in the wild. Further, sequence similarity between distant wild populations suggests recent fragmentation. Collectively, these results point to wild-type declines coinciding with widespread domestication. Second, we hypothesize that the disappearance of large herbivores struck a critical ecological blow against wildCucurbita,and we take initial steps to consider this hypothesis through crossmammal analyses of bitter taste receptor gene repertoires. Directly, megafauna consumedCucurbitafruits and dispersed their seeds; wildCucurbitawere likely left without mutualistic dispersal partners in the Holocene because they are unpalatable to smaller surviving mammals with more bitter taste receptor genes. Indirectly, megafauna maintained mosaic-like landscapes ideal forCucurbita,and vegetative changes following the megafaunal extinctions likely crowded out their disturbed-ground niche. Thus, anthropogenic landscapes provided favorable growth habitats and willing dispersal partners in the wake of ecological upheaval.