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Anthropogenic Seed Dispersal: Rethinking the Origins of Plant Domestication

2020; Elsevier BV; Volume: 25; Issue: 4 Linguagem: Inglês

10.1016/j.tplants.2020.01.005

1878-4372

Robert N. Spengler,

Botany, Ecology, and Taxonomy Studies

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 (74) Google Scholar]. In plants, both intra- and interspecies gene flow push evolution forward [18.Feder J.L. et al.The genomics of speciation-with-gene-flow.Trends Genet. 2012; 28: 342-350Abstract Full Text Full Text PDF PubMed Scopus (461) Google Scholar,19.Garant D. et al.The multifarious effects of dispersal and gene flow on contemporary adaptation.Funct. Ecol. 2007; 21: 434-443Crossref Scopus (359) Google Scholar]. As part of the gene flow system, seed dispersal allows plants to (i) avoid kin (sibling and parent) competition [20.Holt R.D. et al.Theories of niche conservatism and evolution: could exotic species be potential tests?.in: Sax D.F. Stachowicz J.J. Gaines S.D. Species Invasions: Insights into Ecology, Evolution, and Biogeography. Sinauer Associates Inc., 2005: 259-290Google Scholar, 21.Hamilton W.D. May R.M. Dispersal in stable habitats.Nature. 1977; 269: 578-581Crossref Scopus (872) Google Scholar, 22.Ashely M.V. Plant parentage, pollination, and dispersal: How DNA microsatellites have altered the landscape.Crit. Rev. Plant Sci. 2010; 29: 148-169Crossref Scopus (168) Google Scholar], (ii) avoid interspecific competition, (iii) reduce inbreeding [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], and (iv) colonize new areas [23.Venable D.L. Brown J.S. The selective interactions of dispersal, dormancy, and seed size as adaptations for reducing risk in variable environments.Am. Nat. 1988; 131: 360-384Crossref Scopus (690) Google Scholar, 24.Howe H.F. Smallwood J. Ecology of seed dispersal.Annu. Rev. Ecol. Syst. 1982; 13: 201-228Crossref Scopus (2114) Google Scholar, 25.Escribano-Avila G. et al.Diverse guilds provide complementary dispersal services in a woodland expansion process after land abandonment.J. Appl. Ecol. 2014; 51: 1701-1711Crossref Scopus (36) Google Scholar]. Biotic dispersal can also lead to directed dispersal, targeting prime colonization areas and allowing greater offspring success rates than if dispersal were random [26.Eriksson O. Evolution of seed size and biotic seed dispersal in angiosperms: paleoecological and neoecological evidence.Int. J. Plant Sci. 2008; 169: 863-870Crossref Scopus (64) Google Scholar]. Additionally, germination dormancy is seed dispersal through time [27.Cohen D. Optimizing reproduction in a randomly varying environment.J. Theor. Biol. 1966; 12: 119-129Crossref PubMed Scopus (878) Google Scholar]. Following the Janzen-Connell hypothesis, low rates of seed dispersal will lead to high rates of density-dependent mortality [28.Kellner J.R. Hubbell S.P. Density-dependent adult recruitment in a low-density tropical tree.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 11268-11273Crossref PubMed Scopus (14) Google Scholar, 29.Janzen D.H. Herbivores and the number of tree species in tropical forests.Am. Nat. 1970; 104: 501-528Crossref Google Scholar, 30.Connell J.H. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees.in: den Boer P.J. Gradwell G.R. Dynamics of Populations. Center for Agricultural Publishing and Documentation, 1971: 298-312Google Scholar]. Many plants possess both biotic and abiotic dispersal strategies or use multiple dispersal systems [31.Tiffney B.H. Vertebrate dispersal of seed plants through time.Annu. Rev. Ecol. Evol. Syst. 2004; 35: 1-29Crossref Scopus (147) Google Scholar]. However, all plants have evolved ways to move their seeds and spread their genes. Many scholars recognize that these processes are only rarely opportunistic or random, although some scholars see many rapidly growing annuals as having no specific dispersal strategy. Rindos recognized the significance of seed dispersal in the domestication processes, and he cautiously stated that the 'evolution of cultivated plants came about by the development of specialized dispersal relationships between humans and numerous previously opportunistically dispersed plants' ([32.Rindos D. The Origins of Agriculture: An Evolutionary Perspective. Academic Press, 1984Google Scholar], p. 120). Other scholars since then have acknowledged the significance of seed dispersal mechanisms in domestication [33.Fuller D.Q. Allaby R. Seed dispersal and crop domestication: shattering, germination and seasonality in evolution under cultivation.Ann. Plant Rev. 2009; 38: 238-295Google Scholar, 34.Ladizinsky G. Plant Evolution under Domestication. Kluwer Academic Publishers, 1998Crossref Google Scholar, 35.Wood D. Lenné J.M. A natural adaptive syndrome as a model for the origins of cereal agriculture.Proc. Biol. Sci. 2018; 285: 20180277Crossref PubMed Scopus (7) Google Scholar]; however, few of these studies looked beyond the role of tough rachises in large-grained cereal domestication or nondehiscent pods in the domestication of some legumes. In this paper, I argue that all evolution of plants under the first steps toward domestication, during the early and mid-Holocene (before ca. 5000 years ago), was linked to a shift in seed dispersal mechanisms (Table S1 in the supplemental information online and Figure 1). Therefore, domestication is the evolution of new traits in order to support a mutualistic relationship with humans, and it was an inevitable evolutionary response in plants to (i) increasingly more complex human harvesting practices, notably sickle harvesting (seed predation), seed saving, seed trading, and sowing (dispersal); (ii) increased human population size (herbivory pressure); and (iii) sedentism (an evolutionarily significant time scale of continual selective pressure). Substantially, evolution under cultivation is no different from the evolution of mutualism or antiherbivory defenses as a response to any heavy herbivory pressure and is simply an example of keeping pace with the Red Queen [36.Quental T.B. Marshall C.R. How the Red Queen drives terrestrial mammals to extinction.Science. 2013; 6143: 290-292Crossref Scopus (76) Google Scholar]. Scholars recognize the parallel evolution of domestication traits, often called the 'domestication syndrome'; however, it is not always acknowledged that this parallelism is due to similar selective forces associated with herbivory and seed dispersal [33.Fuller D.Q. Allaby R. Seed dispersal and crop domestication: shattering, germination and seasonality in evolution under cultivation.Ann. Plant Rev. 2009; 38: 238-295Google Scholar]. Archaeologists and biologists have studied the switch from the wild to the anthropogenic seed dispersal state in large-seeded cereals and legumes [33.Fuller D.Q. Allaby R. Seed dispersal and crop domestication: shattering, germination and seasonality in evolution under cultivation.Ann. Plant Rev. 2009; 38: 238-295Google Scholar,37.Li L.-F. Olsen K.M. To have and to hold: selection for seed and fruit retention during crop domestication.Curr. Top. Dev. Biol. 2016; 119: 63-109Crossref PubMed Scopus (30) Google Scholar]. They have studied, in detail, the transition from a brittle rachis to a tough rachis and the role of hygroscopic awns (trypanocarpy) in dispersing and burying large grass seeds [35.Wood D. Lenné J.M. A natural adaptive syndrome as a model for the origins of cereal agriculture.Proc. Biol. Sci. 2018; 285: 20180277Crossref PubMed Scopus (7) Google Scholar]. Likewise, studies have illustrated that these cereal crops naturally form dense monodominant fields, which were key for early human harvesting. Greater sibling competition in these dense fields may also have driven evolution of larger seeds with greater offspring provisioning. However, shattering rachises, awns, and dehiscent pods represent only a few of the wild dispersal mechanisms employed by crop progenitors (Figure 2B ). Notably, the majority of domesticated crops were dispersed through animal vectors, most of which were megafaunal mammals (defined here as any animal larger than 40 kg) [38.Janzen D.H. Martin P.S. Neotropical anachronisms: the fruits the gomphotheres ate.Science. 1982; 215: 19-27Crossref PubMed Scopus (508) Google Scholar,39.Janzen D.H. Dispersal of small seeds by big herbivores: foliage is the fruit.Am. Nat. 1984; 123: 338-353Crossref Scopus (283) Google Scholar,64.Spengler III, R.N. Mueller N. Grazing animals drove domestication of grain crops.Nat. Plants. 2019; 5: 656-662Crossref PubMed Scopus (9) Google Scholar]. The effects of the late Pleistocene megafaunal extinctions on these populations have almost completely been overlooked. Janzen and Martin [38.Janzen D.H. Martin P.S. Neotropical anachronisms: the fruits the gomphotheres ate.Science. 1982; 215: 19-27Crossref PubMed Scopus (508) Google Scholar] recognized the megafaunal dispersal mechanism as being significant for many of the fruits that we eat today, and Janzen [39.Janzen D.H. Dispersal of small seeds by big herbivores: foliage is the fruit.Am. Nat. 1984; 123: 338-353Crossref Scopus (283) Google Scholar] went on to illustrate how megafaunal ruminants spread herbaceous plant seeds. The role of seed dispersal in domestication is most evident when looking at the domestication of fruit crops; fleshy fruits are, generally speaking, evolutionary adaptations for dispersing seeds by means of an animal vector. Basic traits of fruiting plant domestication include increases in seed or pit size, pericarp tissue, and concentrations of sugars. In large-fruiting wild plants, these traits evolved to recruit megafaunal dispersers, attracted by large sweet fruits. Despite the metabolic consequences for trees, cucurbits, and Solanaceae plants (solanids), these traits clearly increase overall fitness in an anthropogenic niche; they are also maladaptive under natural selective pressures (nonanthropogenic). Large fruits in most ecosystems today rarely disperse far enough from the parent trees or siblings to pay back the metabolic investment in fruit production. A feral apple tree, for example, often has rotting fruit under it in the fall unless it is located in a horse pasture, and it is plausible that the species might either go extinct or evolve smaller fruits (across the population) without humans. Most large-fruiting crops are effectively obligate domesticates, without the large animal dispersers of the Pleistocene and earlier. Surveys of the progenitors of these large-fruiting trees and cucurbits show that, in most cases, they have small distribution ranges and fragmentary populations, characteristic of range loss and reduced ability to colonize. In general, throughout the Holocene, large-fruiting species of trees have become increasingly restricted in range due to poor seed dispersal [38.Janzen D.H. Martin P.S. Neotropical anachronisms: the fruits the gomphotheres ate.Science. 1982; 215: 19-27Crossref PubMed Scopus (508) Google Scholar,40.Rule S. et al.The aftermath of megafaunal extinction: ecosystem transformation in Pleistocene Australia.Science. 2012; 335: 1483-1486Crossref PubMed Scopus (203) Google Scholar, 41.Pires M.M. et al.Pleistocene megafaunal extinctions and the functional loss of long-distance seed-dispersal services.Ecography. 2017; 41: 153-163Crossref Scopus (61) Google Scholar, 42.Galetti M. et al.Ecological and evolutionary legacy of megafauna extinctions.Biol. Rev. 2017; 93: 845-862Crossref PubMed Scopus (81) Google Scholar, 43.Onstein R.E. et al.To adapt of go extinct? The fate of megafaunal palm fruits under past global change.Proc. R. Soc. B. 2018; 285: 20180882Crossref PubMed Scopus (28) Google Scholar, 44.Guimarães P.R. et al.Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate.PLOS One. 2008; 3e1745Crossref PubMed Scopus (235) Google Scholar, 45.Kistler L. et al.Gourds and squashes (Cucurbita spp.) adapted to megafaunal extinction and ecological anachronism through domestication.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 15107-15112Crossref PubMed Scopus (53) Google Scholar], except in Africa, where large frugivorous dispersers still exist. In some cases, fruits have evolved to be smaller as a response to the loss of large Pleistocene mammalian dispersers [43.Onstein R.E. et al.To adapt of go extinct? The fate of megafaunal palm fruits under past global change.Proc. R. Soc. B. 2018; 285: 20180882Crossref PubMed Scopus (28) Google Scholar]. The lineages of these fruit trees that have survived into the Holocene tend to propagate through shoots and natural cloning rather than via seeds (e.g., Malus sieversii, Prunus mira, Asimina triloba, Maclura pomifera). Often these dense, clonally reproducing wild stands continue to produce extensive generations with energetically costly fruits, which then decompose under the trees, leading to density-dependent seed death through fungal attack, fermentation, seed predation from small animals, or parent/sibling competition. Large fruits coevolved with megafaunal mammals around the world [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,25.Escribano-Avila G. et al.Diverse guilds provide complementary dispersal services in a woodland expansion process after land abandonment.J. Appl. Ecol. 2014; 51: 1701-1711Crossref Scopus (36) Google Scholar], and humans are the most ubiquitous megafaunal mammal to survive the Pleistocene/Holocene boundary. The evolution of even larger fruits and larger seeds under human dispersal is substantially no different from the evolution of large fruits in response to proboscideans (notably gomphotheres), Xenarthra (e.g., Glyptodon spp., megalonychids, megatheriids), Perissodactyl (e.g., rhinoceroses, equids), or earlier large primates. While many mammals coevolved with fruit trees, resulting in seed dispersal–based mutualism, primates are particularly responsible for driving the evolution of larger fruits [46.Sussman R.W. Primate origins and the evolution of angiosperms.Am. J. Primatol. 1991; 23: 209-223Crossref PubMed Scopus (185) Google Scholar,47.Sussman R.W. et al.Rethinking primate origins again.Am. J. Primatol. 2013; 75: 95-106Crossref PubMed Scopus (70) Google Scholar]. Primates can consume and carry large-seeded fruits; in some tropical forests, they are the primary factors in determining forest vegetation communities, essentially creating orchards of primate-dispersed fruit trees [48.Lambert J.E. Graber P.A. Evolutionary and ecological impacts of primate seed dispersal.Am. J. Primatol. 1998; 45: 9-28Crossref PubMed Google Scholar]. High postdigestion germination rates and extensive dispersal distances have been recorded for all great apes, and these megafaunal primates can disperse hundreds of seeds over great distances daily [49.Lambert J.E. Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal.Am. J. Phys. Anthropol. 1999; 109: 365-386Crossref PubMed Scopus (99) Google Scholar]; additionally, they can readily disperse seeds larger than 2.0 cm [50.Wrangham R.W. et al.Seed dispersal by forest chimpanzees in Uganda.J. Trop. Ecol. 1994; 10: 355-368Crossref Scopus (130) Google Scholar]. The coevolutionary bond between primates and large-fruiting angiosperms has been a continuous process since the Eocene [31.Tiffney B.H. Vertebrate dispersal of seed plants through time.Annu. Rev. Ecol. Evol. Syst. 2004; 35: 1-29Crossref Scopus (147) Google Scholar,47.Sussman R.W. et al.Rethinking primate origins again.Am. J. Primatol. 2013; 75: 95-106Crossref PubMed Scopus (70) Google Scholar]; humans are just a recent iteration of this mutualism. Therefore, the evolution of agriculture-type seed dispersal–based mutualism in primates has been developing for at least 40 million years. While monogastric species can pass relatively large seeds, ruminant grazers (Bovidae) have a much more effective digestive system. The restricted cecum of most ruminants, combined with double digestion, heavy mastication, and fermentation, constrains the size and the physiomorphological makeup of seeds that can pass through the digestive system and remain viable [51.Mouissie A.M. et al.Ecological correlates of seed survival after ingestion by fallow white-tailed deer.Funct. Ecol. 2005; 19: 284-290Crossref Scopus (64) Google Scholar,64.Spengler III, R.N. Mueller N. Grazing animals drove domestication of grain crops.Nat. Plants. 2019; 5: 656-662Crossref PubMed Scopus (9) Google Scholar]. Ruminant-dispersed plants are mostly herbaceous, contain hard seed coats, and have small seeds, which are often round with smooth surfaces [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,39.Janzen D.H. Dispersal of small seeds by big herbivores: foliage is the fruit.Am. Nat. 1984; 123: 338-353Crossref Scopus (283) Google Scholar,51.Mouissie A.M. et al.Ecological correlates of seed survival after ingestion by fallow white-tailed deer.Funct. Ecol. 2005; 19: 284-290Crossref Scopus (64) Google Scholar,64.Spengler III, R.N. Mueller N. Grazing animals drove domestication of grain crops.Nat. Plants. 2019; 5: 656-662Crossref PubMed Scopus (9) Google Scholar]. Most of these plants evolved to display seeds on top of their terminal leaves, often lack mechanical dehiscence, and produce abundant generations [52.Pakeman R.J. et al.Ecological correlates of endozoochory by herbivores.Funct. Ecol. 2002; 16: 296-304Crossref Scopus (171) Google Scholar,53.Jacobs B.F. et al.The origin of grass-dominated ecosystems.Ann. Mo. Bot. Gard. 1999; 86: 933-950Crossref Scopus (449) Google Scholar]. The global fossil record shows that annuals diversified and radiated in response to grazing animals during the Miocene, leading to the first grasslands [26.Eriksson O. Evolution of seed size and biotic seed dispersal in angiosperms: paleoecological and neoecological evidence.Int. J. Plant Sci. 2008; 169: 863-870Crossref Scopus (64) Google Scholar,31.Tiffney B.H. Vertebrate dispersal of seed plants through time.Annu. Rev. Ecol. Evol. Syst. 2004; 35: 1-29Crossref Scopus (147) Google Scholar,53.Jacobs B.F. et al.The origin of grass-dominated ecosystems.Ann. Mo. Bot. Gard. 1999; 86: 933-950Crossref Scopus (449) Google Scholar]. Paleogene megafaunal Perissodactyla (including equids, rhinoceroses, and tapirs) were far more likely than true ruminants to disperse large seeds and consume sugary fruits. Artiodactyla (including bison, deer, and their relatives) are responsible for the prominence of small-seeded herbaceous plants that dominate grasslands today [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,54.Nathan R.F.M. et al.Mechanisms of long-distance seed dispersal.Trends Ecol. Evol. 2008; 23: 638-647Abstract Full Text Full Text PDF PubMed Scopus (502) Google Scholar]. In some cases, the evolution of annuals in response to ruminant grazing led to herbivory defenses, such as an increased production of phytoliths or secondary compounds. In other cases, plants evolved mutualistic relationships, such as through seed dispersal. Holocene grasslands are occupied by small herbaceous plants that have phenotypic adaptations to support endozoochoric dispersal. Studies of seed composition in herbivore dung and seed germination rates postdigestion illustrate that many progenitors were dispersed by mammalian megafaunal grazers [51.Mouissie A.M. et al.Ecological correlates of seed survival after ingestion by fallow white-tailed deer.Funct. Ecol. 2005; 19: 284-290Crossref Scopus (64) Google Scholar,64.Spengler III, R.N. Mueller N. Grazing animals drove domestication of grain crops.Nat. Plants. 2019; 5: 656-662Crossref PubMed Scopus (9) Google Scholar]. Larger seed sizes and greater provisioning allow plants to outcompete their neighbors; however, seed size is often constrained by dispersal mechanisms and seed predation rates [31.Tiffney B.H. Vertebrate dispersal of seed plants through time.Annu. Rev. Ecol. Evol. Syst. 2004; 35: 1-29Crossref Scopus (147) Google Scholar]. The constraint of the ruminant dispersal mechanism (rarely passing viable seeds larger than 2.0 mm) is one factor explaining why so many of our noncereal grains are small today. Some examples of modern crops that had progenitors with ruminant seed dispersal traits include chenopods (Chenopodium spp.), most of our millets, buckwheat (Fagopyrum spp.), maize (Zea mays), hemp (Cannabis sativa), and most of the lost crops of the Eastern Agricultural Complex [55.Small E. Evolution and classification of Cannabis sativa (marijuana, hemp) in relation to human u