Emerging evidence of plant domestication as a landscape-level process
Authors: Robin G. Allaby, Chris J. Stevens, Logan Kistler, Dorian Q. Fuller
Journal: Trends in Ecology & Evolution (2021)

Current theories of plant domestication are based on localized founder models in which single or multiple domestications occur as a progressive result of adaptation processes, but anomalies that do not fit within this perspective have been accumulating.We describe developments in archaeology and genetics over the past decade in which cultural connections between groups stretch back much further in time than was previously realized, and over wide geographic distances. Weak selection for domestication substantially pre-dates domestication and/or cultivation practices, large populations appear to have been maintained throughout the emergence of domesticates, and the resulting forms were not necessarily an improvement in terms of yield.We present a framework in which the process of domestication evolved as a landscape-level process involving large populations connected through sustained long-term human contact over large distances from which domesticate forms emerged in a complex manner as an adaptive reaction to long-term exploitation that did not necessarily provide immediate benefits.The landscape framework addresses several anomalies and radically changes the dynamic visualization of the evolution of domestication. It also opens up a list of new questions regarding the mechanisms of selection and the assembly of domestication syndrome alleles, and obliges a profound rethink of the progressive nature of domestication and human cultural evolution. The evidence from ancient crops over the past decade challenges some of our most basic assumptions about the process of domestication. The emergence of crops has been viewed as a technologically progressive process in which single or multiple localized populations adapt to human environments in response to cultivation. By contrast, new genetic and archaeological evidence reveals a slow process that involved large populations over wide areas with unexpectedly sustained cultural connections in deep time. We review evidence that calls for a new landscape framework of crop origins. Evolutionary processes operate across vast distances of landscape and time, and the origins of domesticates are complex. The domestication bottleneck is a redundant concept and the progressive nature of domestication is in doubt. The evidence from ancient crops over the past decade challenges some of our most basic assumptions about the process of domestication. The emergence of crops has been viewed as a technologically progressive process in which single or multiple localized populations adapt to human environments in response to cultivation. By contrast, new genetic and archaeological evidence reveals a slow process that involved large populations over wide areas with unexpectedly sustained cultural connections in deep time. We review evidence that calls for a new landscape framework of crop origins. Evolutionary processes operate across vast distances of landscape and time, and the origins of domesticates are complex. The domestication bottleneck is a redundant concept and the progressive nature of domestication is in doubt. The evolution of domesticated (see Glossary) plants underpinning the rise of agriculture is often seen as a pivotal moment in human progress, but the process was also associated with the initial costs of malnutrition [1.Larsen C.S. Biological changes in human populations with agriculture.Annu. Rev. 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We are increasingly appreciating the complexities involved in the evolution of domestication [4.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 (371) Google Scholar,5.Purugganan M. Evolutionary insights into the nature of plant domestication.Curr. Biol. 2019; 29: R705-R714Abstract Full Text Full Text PDF PubMed Scopus (82) Google Scholar]. A decade ago saw a shift in thinking from simple single-localized crop origins to more complex origins [6.Brown T.A. et al.The complex origins of domesticated crops.Trends Ecol. Evol. 2009; 24: 103-109Abstract Full Text Full Text PDF PubMed Scopus (198) Google Scholar]. Recently, increasingly diverse disciplines have contributed evidence highlighting the complexity of domestication. In parallel cases, domestication occurred over vast but culturally connected distances, over long periods of time, and initially in periods long before early agriculture. This evidence resets the frame of the debate as emerging data reveal that domestication does not fit with conventional visualizations of the process (Figure 1) . The consequences for the interpretation of cultural shifts are potentially profound, and will require rethinking of how human societies evolved with so far underappreciated levels of long-distance social interaction that allowed exchange of plant germplasm and knowledge. We detail below aspects of the plant domestication process that have come under revision through emerging archaeogenomic and archaeobotanical evidence. We conclude that a landscape perspective will be necessary, as visualized in Figure 2, to frame domestication research in a way that incorporates current anomalies to the conventional view. The progression of domestication can be tracked from the archaeological record through observation of changes in the key visible traits of the domestication syndrome. These traits include seed size and dispersal (shattering) in crops such as cereals. In many species seeds transition to larger dimensions with the rise of domesticated forms [1.Larsen C.S. Biological changes in human populations with agriculture.Annu. Rev. Anthropol. 1995; 24: 185-213Crossref Google Scholar,7.Fuller D. Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World.Ann. Bot. 2007; 100: 903-924Crossref PubMed Scopus (469) Google Scholar]. Seed-shattering changes are evident in abscission scar morphology where jagged forms indicate the threshing of Southwestern Asiatic cereals (einkorn, Triticum monococcum; emmer, Triticum dicoccum; and barley, Hordeum vulgare) and rice (Oryza sativa) in the Lower Yangtze [7.Fuller D. 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This phenomenon is seen for all early crops in the Fertile Crescent [12.Arranz-Otaegui A. et al.Regional diversity on the timing for the initial appearance of cereal cultivation and domestication in southwest Asia.Proc. Natl. Acad. Sci. U. S. A. 2016; 113: 14001-14006Crossref PubMed Scopus (46) Google Scholar,15.Fuller D.Q. et al.Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record.Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 6147-6152Crossref PubMed Scopus (223) Google Scholar,20.Fuller D.Q. et al.Cultivation and domestication had multiple origins: arguments against the core area hypothesis for the origins of agriculture in the Near East.World Archaeol. 2011; 43: 628-652Crossref Scopus (119) Google Scholar] and East Asia [21.Ren X. et al.Foothills and intermountain basins: does China's Fertile Arc have 'Hilly Flanks'?.Quat. Int. 2016; 426: 86-96Crossref Scopus (20) Google Scholar,22.Stevens C.J. Fuller D.Q. 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It was first established that, for the cereals of Southwest Asia (einkorn, emmer, barley) and East Asia (rice), the selection coefficients for both traits were very low, and, crucially, were comparable to those involved in natural selection [23.Purugganan M.D. Fuller D.Q. The nature of selection during plant domestication.Nature. 2009; 457: 843-848Crossref PubMed Scopus (557) Google Scholar,24.Purugganan M.D. Fuller D.Q. Archaeological data reveal slow rates of evolution during plant domestication.Evolution. 2011; 65: 171-183Crossref PubMed Scopus (124) Google Scholar]. This observation was similarly found in a wider range of crops, including lentils, goosefoot, mung-bean, sunflower, soybean, pea, and squash [15.Fuller D.Q. et al.Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record.Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 6147-6152Crossref PubMed Scopus (223) Google Scholar]. Such findings question the notion that strong artificial selection associated with early domestication was a general principle, and this has implications for the modes and mechanisms of selection involved. Further dissection of the strength of selection established that selection pressures changed over time [25.Allaby R.G. et al.Geographic mosaics and changing rates of cereal domestication.Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2017; 2: 20160429Crossref Scopus (45) Google Scholar]. Notably in the case of Southwest Asian cereals (einkorn, emmer, barley) a strong increase in selection is associated with the development and increasing dominance of stone sickle technologies [26.Maeda O. et al.Narrowing the harvest: increasing sickle investment and the rise of domesticated cereal agriculture in the Fertile Crescent.Quat. Sci. Rev. 2016; 145: 226-237Crossref Scopus (46) Google Scholar]. 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Most domestication researchers now recognize the teleological paradox that conscious initial domestication engenders: proto-agriculturalists would need to recognize traits and predict the complex consequences of breeding before having ever achieved it. It further requires an ability to identify very low frequencies of extremely subtle differences between plants, a scenario that most find unconvincing. However, the notion of selective breeding has deep roots in biological thought. Darwin first used it to demonstrate the principal of natural selection [44.Darwin C. Variation under domestication.in: Origin of Species. Murray, 1859: 7-43Google Scholar], although he attributed the domestication process itself to unintentional selection biases [45.Darwin C. Variation of Plants and Animals under Domestication. Murray, 1869: 114Google Scholar]. Later it was invoked in the guise of truncation selection as a possible general mode of selection [46.Sved J.A. Possible rates of gene substitution in evolution.Am. Nat. 1968; 102: 283-293Crossref Google Scholar]. The latter was identified as a highly efficient mechanism of selection that largely avoids the selection costs caused by genetic load under conventional environmental selection models (Box 1) [48.Crow J.F. Kimura M. Efficiency of truncation selection.Proc. Natl. Acad. Sci. U. S. A. 1979; 76: 396-399Crossref PubMed Scopus (118) Google Scholar,49.Barton N.H. Linkage and the limits to natural selection.Genetics. 1995; 140: 821-841Crossref PubMed Google Scholar]. Although truncation selection operates in selective breeding, it is questionable whether the ranking and truncation it requires (Box 1) could occur in nature [48.Crow J.F. Kimura M. Efficiency of truncation selection.Proc. Natl. Acad. Sci. U. S. A. 1979; 76: 396-399Crossref PubMed Scopus (118) Google Scholar], and, given the lack of natural empirical examples, it is likely to be vanishingly rare if it exists at all.Box 1Models of selectionSelection models are invoked to describe mechanisms of selection that remove less-fit individuals. Many models apply Haldane's original approach [47.Haldane J.B.S. The cost of selection.J. Genet. 1957; 55: 511-524Crossref Scopus (370) Google Scholar] of environmental degradation (Figure IA) in which an environmental factor challenges the population such that the majority is suddenly at a selective disadvantage, and a genetic load is therefore imposed. Mutations that overcome the challenge rise in frequency while wild types have a probability of extinction that is expressed by the magnitude of the selection coefficient (S in Figure I). The resulting reduction in population size during selection is the substitution load. Strong selection can rapidly lead to the demise of the population, and numerous simultaneous adaptive challenges rapidly bring maximum possible selection strengths to nearly neutral levels [54.Allaby R.G. et al.Surprisingly low limits of selection in plant domestication.Evol. Bioinforma. 2015; 11: 41-51PubMed Google Scholar] even when multiple adaptive solutions are available, an initial criticism of Haldane's approach [55.Maynard-Smith J. 'Haldane's dilemma' and the rate of evolution.Nature. 1968; 219: 1114-1116Crossref PubMed Scopus (61) Google Scholar, 56.Felsenstein J. On the biological significance of the cost of gene substitution.Am. Nat. 1971; 105: 1-11Crossref Google Scholar, 57.Barton N. Partridge L. Limits to natural selection.Bioessays. 2000; 22: 1075-1084Crossref PubMed Scopus (150) Google Scholar]. The standard stabilizing selection model is a subset of environmental selection that is often applied to complex traits [65.Barton N.H. The maintenance of polygenic variation through a balance between mutation and stabilizing selection.Genet. Res. Camb. 1986; 47: 209-216Crossref PubMed Scopus (95) Google Scholar]. This model accounts for the increasing fitness of individuals as numerous loci involved in a single adaptive challenge gain adaptive alleles. Here the strength of selection necessarily diminishes as individuals approach the fitness threshold, and hence will always behave as stabilizing selection.Selective breeding works through the alternative mechanism of truncation selection (Figure IB) in which individuals are ranked by fitness with respect to a particular trait, and again a fitness threshold is imposed [46.Sved J.A. Possible rates of gene substitution in evolution.Am. Nat. 1968; 102: 283-293Crossref Google Scholar]. In contrast to Haldane's selection, all individuals below the threshold are removed, and all individuals above are retained. Because the fitness threshold can be placed in a way that predictably splits the population, such as retaining the top half while discarding the lower half, the extent to which the population is reduced can be controlled and the problem of the substitution load becoming excessive is overcome [48.Crow J.F. Kimura M. Efficiency of truncation selection.Proc. Natl. Acad. Sci. U. S. A. 1979; 76: 396-399Crossref PubMed Scopus (118) Google Scholar].A third class of selection model differs from Haldane's original system in that the strength of selection is a dynamic function of individuals of the population rather than the environment. These often work by frequency- or density-dependency. One such example is competitive selection [68.Allaby R.G. et al.A novel cost framework reveals evidence for competitive selection in the evolution of complex traits during plant domestication.BioRxiv. 2020; (Published online October 31, 2020)https://doi.org/10.1101/2020.10.30.362236Google Scholar] (Figure IC). Here an advantage is gained by a mutant in resource acquisition. This increase in resource acquisition elicits a burden shared by the remainder of the population. As more advantaged individuals appear, resource becomes rarer for the wild type, thus intensifying their selective removal, and the excess resource diminishes with increasing competition between advantaged individuals until the population returns to its original state. Selection models are invoked to describe mechanisms of selection that remove less-fit individuals. Many models apply Haldane's original approach [47.Haldane J.B.S. The cost of selection.J. Genet. 1957; 55: 511-524Crossref Scopus (370) Google Scholar] of environmental degradation (Figure IA) in which an environmental factor challenges the population such that the majority is suddenly at a selective disadvantage, and a genetic load is therefore imposed. Mutations that overcome the challenge rise in frequency while wild types have a probability of extinction that is expressed by the magnitude of the selection coefficient (S in Figure I). The resulting reduction in population size during selection is the substitution load. Strong selection can rapidly lead to the demise of the population, and numerous simultaneous adaptive challenges rapidly bring maximum possible selection strengths to nearly neutral levels [54.Allaby R.G. et al.Surprisingly low limits of selection in plant domestication.Evol. Bioinforma. 2015; 11: 41-51PubMed Google Scholar] even when multiple adaptive solutions are available, an initial criticism of Haldane's approach [55.Maynard-Smith J. 'Haldane's dilemma' and the rate of evolution.Nature. 1968; 219: 1114-1116Crossref PubMed Scopus (61) Google Scholar, 56.Felsenstein J. On the biological significance of the cost of gene substitution.Am. Nat. 1971; 105: 1-11Crossref Google Scholar, 57.Barton N. Partridge L. Limits to natural selection.Bioessays. 2000; 22: 1075-1084Crossref PubMed Scopus (150) Google Scholar]. The standard stabilizing selection model is a subset of environmental selection that is often applied to complex traits [65.Barton N.H. The maintenance of polygenic variation through a balance between mutation and stabilizing selection.Genet. Res. Camb. 1986; 47: 209-216Crossref PubMed Scopus (95) Google Scholar]. This model accounts for the increasing fitness of