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

Abstract

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 crossmammal 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.evolutionary ecology | sensory ecology | TAS2R genes | ancient DNA | archaeogenomics

Ecology of a widespread large omnivore, Homo sapiens, and its impacts on ecosystem processes

“…Since a comprehensive review of H. sapiens hunter-gatherer ecological roles would include the entire fields of ethnography, human ecology, and archaeology, we do not claim to be exhaustive. For some plants, H. sapiens appears to have emerged as a substitute mutualistic partner after the extinction of megafauna (Kistler et al, 2015). The hunter-gatherer phenotype (as well as along the gradient toward agricultural strategies) has many commensal and mutualistic species, which benefit from H. sapiens disturbances and niche construction (Diamond, 2002;Keller, 2007;Lundholm & Richardson, 2010).…”

“…It also ignores that they have previously, over evolutionary time, taken over the ecological roles of extinct species and are thus capable of doing so in the future (Kistler et al, 2015). Despite widespread concern over the increasing negative environmental impacts of agriculturalist H. sapiens, almost no attention has been paid to the extinction of other ecological roles that this uniquely flexible species once played.…”

The Rise of the Anthroposphere since 50,000 Years: An Ecological Replacement of Megaherbivores by Humans in Terrestrial Ecosystems?

“…Elephant and rhinoceros damage trees (Schüle, 1992;Omeja et al, 2014;Terborgh et al, 2016) Large scale deforestation to gain forage areas for domestic herbivores and crop fields (Godwin, 1944;Williams, 2008) Nutrient cycling and fertilization Recycling and spreading of nutrients away from hotspots and counteracting gravity Doughty et al, 2013Doughty et al, , 2016b Active fertilization of agricultural areas: manuring, plowing, cultivation of legumes in rotation (Galloway et al, 2013); recycling human and animal waste (Melillo, 2012); increasing P export (Boyle et al, 2015) Megafruit and seed dispersal Promoting dispersal of plants with megaseeds (Guix, 2009;Corlett, 2013) Domestication of megafruit plant species (e.g., avocado, chocolate, squashes Kistler et al, 2015) Emissions of greenhouse gas Methane emissions through digestive fermentation (Smith et al, 2016a) CO 2 emissions through forest clearing (Ruddiman and Ellis, 2009). Methane emissions by domestic ruminants, rice paddies (Fuller et al, 2011) In some cases, humans have limited the negative impact of the loss of megaherbivores for the plant species producing very large fruits and they behaved as a partial replacement of large fruits dispersers (Guimarães et al, 2008).…”

“…Methane emissions by domestic ruminants, rice paddies (Fuller et al, 2011) In some cases, humans have limited the negative impact of the loss of megaherbivores for the plant species producing very large fruits and they behaved as a partial replacement of large fruits dispersers (Guimarães et al, 2008). For plant species such as gourds and squashes, chocolate and avocado that became cultivated by humans, changing fruit and seed disperser led probably to an increase of the range of the species (Landon, 2009;Kistler et al, 2015).…”

The efficacy of high-throughput sequencing and target enrichment on charred archaeobotanical remains

“…High-throughput sequencing (HTS) overcomes this limitation, allowing for sequencing of very short DNA fragments27. Moreover, techniques such as target enrichment now allow for the preferential sequencing of DNA sequences of interest, regardless of fragment length2829303132. Owing to these benefits, a combination of these techniques has been suggested as the future method of choice when working with charred, archaeobotanical material28.…”