Monday, November 21, 2016

Pumpkin History

Happy Thanksgiving (with a hat tip to CNN)!

Pre-Columbian hunters and gatherers may have proto-farmed pumpkins, squash and gourds, which were domesticated in the Americas, after their survival was threatened by the megafauna extinction caused by their arrival in the Americas. 

Squashes, pumpkins, and gourds belonging to the genus Cucurbita were domesticated on several occasions throughout the Americas, beginning around 10,000 years ago. The wild forms of these species are unpalatably bitter to humans and other extant mammals, but their seeds are present in mastodon dung deposits, demonstrating that they may have been dispersed by large-bodied herbivores undeterred by their bitterness. However, Cucurbita may have been poorly adapted to a landscape lacking these large dispersal partners. Our study proposes a link between the disappearance of megafaunal mammals from the landscape, the decline of wild Cucurbita populations, and, ultimately, the evolution of domesticated Cucurbita alongside human cultivators. 
The genus Cucurbita (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 wild Cucurbita, 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 total Cucurbita samples, comprising ancient (n = 19), modern wild (n= 30), and modern 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 wild Cucurbita, and we take initial steps to consider this hypothesis through cross-mammal analyses of bitter taste receptor gene repertoires. Directly, megafauna consumed Cucurbita fruits and dispersed their seeds; wild Cucurbita were 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 for Cucurbita, 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.

Pumpkins, squashes and gourds were domesticated by pre-Columbian Native Americans many thousands of years ago from five different wild species, three of which still exist today and two of which have no known wild ancestors that still exist. Genetic evidence shows no evidence of crossing of subspecies of Cucurbita. The family tree of these plant sub-species is as follows:

Genetic relationships among 104 accessions of Cucurbita pepo were assessed from polymorphisms in 134 SSR (microsatellite) and four SCAR loci, yielding a total of 418 alleles, distributed among all 20 linkage groups. Genetic distance values were calculated, a dendrogram constructed, and principal coordinate analyses conducted. The results showed 100 of the accessions as distributed among three clusters representing each of the recognized subspecies, pepo, texana, and fraterna. The remaining four accessions, all having very small, round, striped fruits, assumed central positions between the two cultivated subspecies, pepo and texana, suggesting that they are relicts of undescribed wild ancestors of the two domesticated subspecies. In both, subsp. texana and subsp. pepo, accessions belonging to the same cultivar-group (fruit shape) associated with one another. Within subsp. pepo, accessions grown for their seeds or that are generalists, used for both seed and fruit consumption, assumed central positions. Specialized accessions, grown exclusively for consumption of their young fruits, or their mature fruit flesh, or seed oil extraction, tended to assume outlying positions, and the different specializations radiated outward from the center in different directions. Accessions of the longest-fruited cultivar-group, Cocozelle, radiated bidirectionally, indicating independent selection events for long fruits in subsp. pepo probably driven by a common desire to consume the young fruits. Among the accessions tested, there was no evidence for crossing between subspecies after domestication.

The conclusion of the 2011 paper notes that:
Before domestication, Cucurbita pepo evolved into three lineages, subsp. fraterna, which grows wild in northeastern Mexico, subsp. texana, which grows wild in the southeastern United States, and subsp. pepo, which has not been discovered in the wild but may have originated in southern North America. Ornamental cultigens producing the smallest, round, striped fruits are located centrally between subsp. texana and subsp. pepo, suggesting that they are relicts of unknown wild progenitors. No cultigens closely related to subsp. fraterna have been identified. After domestication and long before the arrival of Europeans, subsp. texana evolved into several edible-fruited cultivar-groups characterized by fruit shapes deviating from roundness. In subsp. pepo, the evolution of long-fruited cultivar-groups is more recent and occurred primarily in Europe. Although there is no obvious genetic barrier to crossing among the subspecies, none of the cultivar-groups and none of the accessions examined appears to derive from such crossing.
The body of the 2011 paper notes that:
Cucurbita pepo subsp. texana is divided into distinct sub-clusters​, four of which are based on the edible-fruited cultivar-groups that were defined by fruit shape and named Acorn, Crookneck, Scallop, and Straightneck (Paris 1986). . . . the Scallop Group (T-SC) in the most central position within Cucurbita pepo subsp. texana and, of the edible-fruited cultivar-groups, closest to the wild (T-GT) gourds. Thus, it appears likely that it was the first edible-fruited cultivar-group to have evolved and diversified under the guidance of the pre-Columbian, Native Americans of what is now the United States. Findings of rind fragments of different fruit forms, including lobed, furrowed, and warted, at sites 2,500–3,000 years old in Kentucky, are suggestive of incipient differentiation into the Scallop (T-SC), Acorn (T-AC), and Crookneck (T-CN) Groups (Watson and Yarnell 1966, 1969; Cowan 1997). These three cultivar-groups can be thought of as products of pre-Columbian genetic drift and conservation in isolation that occurred in eastern North America. The Straightneck Group (T-SN) appears to be a much more recent development, judging from the low average GD value among straightneck cultivars (Table 2), consistent with its absence from the historical record prior to the late nineteenth century (Paris 2000a). Earlier results suggested that the Straightneck Group was derived from a cross between a cultivar of the Crookneck Group and a cultivar of the Acorn Group (Paris et al. 2003), but the present results favor a direct derivation from the Crookneck Group. . . .  
The five accessions of the Zucchini Group (ZU) are very closely related, having the lowest within-group GD value. The zucchinis form a distinct sub-cluster, as already observed using other markers. Another sub-cluster is formed by the three accessions representing a market type within the Pumpkin Group (PU), the oil-seed pumpkins, P-PU-GLE, P-PU-STY, and P-PU-WIE. Both, the zucchinis and the oil-seed pumpkins have a short history. The Zucchini Group apparently originated in the environs of Milan in the late nineteenth century (Paris 2000a). The oil-seed pumpkins derive from a recessive, hull-less mutation that occurred in Styria, Austria in the 1880s (Teppner 2000). The Pumpkin Group, the Vegetable Marrow Group (P-VM), and the Cocozelle Group (P-CO), which have considerably longer histories (Paris 2000a), have high within-group GD values and relative high heterozygosities . . . . .  
Even though domestication of subsp. pepo is thought to precede that of subsp. texana by approximately 5,000 years (Smith 2006), selection for deviation from fruit roundness occurred over 2,000 years earlier in subsp. texana, as indicated by rind fragments found in Kentucky.

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