Anthropogenic Seed Dispersal: Rethinking the Origins of Plant Domestication

Abstract

Archaeobotanical and genetic evidence demonstrates that the first morphological changes in all of the earliest domesticated plants were associated with wild seed dispersal strategies that were no longer advantageous under human cultivation.Domestication was/is a natural response of plants to heavy seed predation by humans. Many plants in the wild have formed a similar seed dispersal–based mutualism with animals as a response to herbivory.Rather than viewing domestication as an intentional human-driven process, domestication is best modeled as a natural evolutionary response to herbivory. Early domestication traits gave plants a selective advantage through the recruitment of humans as seed dispersers.Many of the progenitors of our modern domesticated crops relied on animals for seed dispersal. The natural dispersal processes of many of these crop progenitors were weakened by megafaunal extinctions. It is well documented that ancient sickle harvesting led to tough rachises, but the other seed dispersal properties in crop progenitors are rarely discussed. The first steps toward domestication are evolutionary responses for the recruitment of humans as dispersers. Seed dispersal–based mutualism evolved from heavy human herbivory or seed predation. Plants that evolved traits to support human-mediated seed dispersal express greater fitness in increasingly anthropogenic ecosystems. The loss of dormancy, reduction in seed coat thickness, increased seed size, pericarp density, and sugar concentration all led to more-focused seed dispersal through seed saving and sowing. Some of the earliest plants to evolve domestication traits had weak seed dispersal processes in the wild, often due to the extinction of animal dispersers or short-distance mechanical dispersal. It is well documented that ancient sickle harvesting led to tough rachises, but the other seed dispersal properties in crop progenitors are rarely discussed. The first steps toward domestication are evolutionary responses for the recruitment of humans as dispersers. Seed dispersal–based mutualism evolved from heavy human herbivory or seed predation. Plants that evolved traits to support human-mediated seed dispersal express greater fitness in increasingly anthropogenic ecosystems. The loss of dormancy, reduction in seed coat thickness, increased seed size, pericarp density, and sugar concentration all led to more-focused seed dispersal through seed saving and sowing. Some of the earliest plants to evolve domestication traits had weak seed dispersal processes in the wild, often due to the extinction of animal dispersers or short-distance mechanical dispersal. The linked questions of why, how, when, and where people first domesticated plants and animals are among the greatest mysteries in the development of human culture. Understanding how and why humans gained the ability to produce grain surpluses is the key to understanding the specialization of artistic and intellectual pursuits, as well as the demographic changes that led to the formation of cities and empires. Over the past century, scientists have made great strides in answering the questions of when and where plants first evolved in response to human selective pressures [1.Larson G. et al.Current perspectives and the future of domestication studies.Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 6139-6146Crossref PubMed Scopus (306) Google Scholar,2.Langlie B.S. et al.Agricultural origins from the ground up: archaeological approaches to plant domestication.Am. J. Bot. 2014; 101: 1601-1617Crossref PubMed Scopus (18) Google Scholar]. However, there remains no clear consensus regarding the why and how questions [2.Langlie B.S. et al.Agricultural origins from the ground up: archaeological approaches to plant domestication.Am. J. Bot. 2014; 101: 1601-1617Crossref PubMed Scopus (18) Google Scholar,3.Zeder M.A. Smith B.D. A conversation on agricultural origins: talking past each other in a crowded room.Curr. Anthropol. 2009; 50: 681-691Crossref Scopus (63) Google Scholar]. The lack of agreement may be due to the way these two questions have been framed since Darwin presented the concept of ‘artificial selection’ as opposite to or separate from natural processes [4.Darwin C.R. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, 1859Crossref Google Scholar]. Thinking of domestication as unique from other evolutionary processes effectively makes the why and how questions unanswerable – the greatest trick questions in the sciences. The focus on human agency in the process has left scholars from Pumpelly [5.Pumpelly R. Explorations in Turkestan: Expedition of 1904 Prehistoric Civilizations of Anau: Origins, Growth, and Influence of Environment. Carnegie Institution of Washington, 1908Crossref Google Scholar] and Childe [6.Childe V.G. Man Makes Himself. Watts, 1936Google Scholar] to Sauer [7.Sauer C.O. Agricultural Origins and Dispersals.1952Google Scholar], Cohen [8.Cohen M. The Food Crisis in Prehistory: Overpopulation and the Origins of Agriculture. Yale University Press, 1977Google Scholar], Flannery [9.Flannery K.V. The origins of agriculture.Annu. Rev. Anthropol. 1973; 2: 271-310Crossref Google Scholar], Hayden [10.Hayden B. Nimrods, piscators, pluckers and planters: the emergence of food production.J. Anthropol. Archaeol. 1990; 9: 31-69Crossref Scopus (267) Google Scholar], and hundreds of others searching for rational drivers of human innovation. After 160 years of research into the origins of agriculture, most scholars finally accept that the process was not driven by conscious selection; in accepting this, the scholarly community is poised to reframe the study of evolution under cultivation and focus on the effects of heavy human herbivory on plant communities in the early and mid-Holocene. In this paper, I argue that plant domestication originated through the evolution of those traits which facilitated a stronger mutualistic bond between plants and people, with humans providing seed dispersal services. Evolutionary studies illustrate that mutualism often evolves from a predatory relationship [11.Nathan R. Muller-Landau H.C. Spatial patterns of seed dispersal, their determinants and consequences for recruitment.Trends Ecol. Evol. 2000; 15: 278-285Abstract Full Text Full Text PDF PubMed Scopus (1451) Google Scholar,12.Jara-Guerrero A. et al.White-tailed deer as the last megafauna dispersing seeds in neotropical dry forests: the role of fruit and seed traits.Biotropica. 2018; 50: 169-179Crossref Scopus (15) Google Scholar]. In some cases, plants evolved sugar-rich fruits in order to recruit dispersers, and in other cases, dispersers were enticed by the green foliage that surrounded small, dry-fruited seeds. The process of plants in the wild evolving new traits in order to change their seed dispersal mechanism is effectively the same process that led to morphological changes in seeds during the first few millennia of human cultivation. As an evolutionary process, domestication is governed by the same drivers as all evolution. Ellstrand [13.Ellstrand N.C. Is gene flow the most important evolutionary force in plants?.Am. J. Bot. 2014; 101: 737-753Crossref PubMed Scopus (157) Google Scholar] recently mused that gene flow, as the incorporation of new alleles between genetically differentiated populations, is one of the strongest evolutionary forces in plants and is facilitated by seed dispersal. Studies show that low levels of gene flow often counteract the effects of mutation, genetic drift, and selection [13.Ellstrand N.C. Is gene flow the most important evolutionary force in plants?.Am. J. Bot. 2014; 101: 737-753Crossref PubMed Scopus (157) Google Scholar]. Gene flow can act to make a population more homogenous, or it can lead to genetic variation [14.Mayr E. Animal Species and Evolution. Harvard University Press, 1963Crossref Google Scholar]. Rates of gene flow vary across space, through time, and between specific individuals [13.Ellstrand N.C. Is gene flow the most important evolutionary force in plants?.Am. J. Bot. 2014; 101: 737-753Crossref PubMed Scopus (157) Google Scholar]. However, it is a necessary process for ensuring a healthy population, promoting diversification, adaptive evolution, and overall fitness [15.Hansson B. et al.Heritability of dispersal in the great reed warbler.Ecol. Lett. 2003; 6: 290-294Crossref Scopus (55) Google Scholar, 16.Clobert J. et al.Dispersal. Oxford University Press, 2001Google Scholar, 17.Pasinelli G. et al.Genetic and environmental influences on natal dispersal distance in a resident bird species.Am. Nat. 2004; 164: 660-669Crossref PubMed Scopus Google Scholar]. In and gene flow evolution et of Full Text Full Text PDF PubMed Scopus Google et effects of dispersal and gene flow on Ecol. Scopus Google Scholar]. As of the gene flow seed dispersal plants to and et of and be Species into and Scholar, in Scopus Google Scholar, and have the Rev. Sci. Scopus Google Scholar], [11.Nathan R. Muller-Landau H.C. Spatial patterns of seed dispersal, their determinants and consequences for recruitment.Trends Ecol. 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