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Rethinking the Origins of Agriculture
Human Behavioral Ecology, Phenotypic (Developmental) Plasticity, and Agricultural Origins Insights from the Emerging Evolutionary Synthesis by Kristen J. Gremillion and Dolores R. Piperno The fields of human behavioral ecology (HBE) and evolutionary developmental biology (evo-devo) both stand to make significant contributions to our understanding of agricultural origins. These two approaches share a concern with phenotypic plasticity and its evolutionary significance. HBE considers the adaptive plasticity of the human phenotype in response to resource distribution in time and space and has helped to advance understanding of the economic costs and benefits of food production. However, evo-devo and the associated subject of phenotypic (developmental) plasticity have so far been largely neglected as sources of insight into the domestication of plants, despite growing evidence for their evolutionary importance in nature and their roles in the origins of novel traits. We argue that it is important to consider environmentally induced phenotypic variation resulting directly from both natural- and human-induced ecological change as a source of the distinctive morphologies of domesticated plants.
Human Behavioral Ecology and Agricultural Origins Working with archaeobotanical data from two different New World regions, we have both found human behavioral ecology (HBE) of great value as a heuristic tool for understanding food production as an adaptation. Our logic for our use of HBE (an outgrowth of behavioral ecology [BE]) in modeling and ultimately deriving explanations for the origins and dispersals of food production follows from the following particularly lucid description: “Critics may object to BE’s inherent reductionism and implicit rejection of ‘culture’ as an explanation for human behavior. In our view, these are among
Kristen J. Gremillion is Associate Professor in the Department of Anthropology at the Ohio State University (4034 Smith Laboratory, 174 West 18th Avenue, Columbus, Ohio 43210-1106, U.S.A. [
[email protected]]). Dolores R. Piperno is Senior Scientist and Curator of Archaeobotany and South American Archaeology in the Archaeobiology Program in the Department of Anthropology of the Smithsonian National Museum of Natural History (10th Street and Constitution Avenue, Washington, DC 20560, U.S.A. [pipernod@ si.edu]). This paper was submitted 19 IX 08 and accepted 1 V 09.
its most important virtues. Reducing a problem to its key elements and attacking them one at a time is the essence of good science: It is the most effective way of eliminating problematic answers and identifying and pursuing more promising ones. One might argue that most of BE as applied to humans pertains to ‘culture,’ but unlike many schools of thought in anthropology, BE generally attempts to explain patterns in cultural behavior rather than explain them away as a function of culture” (Bird and O’Connell 2006, 171). We feel that this focus on individual decisions holds great explanatory power by placing human agency at the forefront of explanation. The trends that we infer from the archaeological record represent the cumulative expression in material form of multitudes of decisions made by individuals, whether alone or in groups. Underlying these decisions are complex mechanisms of individual and social learning that have been shaped by millennia of natural selection to yield a highly flexible system of phenotypic adjustment to varying environmental conditions. HBE provides a rigorous methodology for understanding these diverse behavioral responses in evolutionary terms. We begin our discussion of HBE and agricultural origins with a review of some of the successes and failures of the diet
䉷 2009 by The Wenner-Gren Foundation for Anthropological Research. All rights reserved. 0011-3204/2009/5005-0005$10.00. DOI: 10.1086/605360
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breadth model, a venerable and robust model that has yielded important insights into food choice in many species, including humans (Bettinger 1987; Bird and O’Connell 2006; Kelly 1995; Stephens and Krebs 1986). We will not attempt a full description of the model here but instead focus on some of its predictions that have particular relevance for the practice of food production. The most important of these is that as highly ranked resources become scarce, the cost of continuing to search for them rises to the point at which it is more efficient overall to be less selective and to accept other less profitable resources into the diet. The implication is that food scarcity tends to encourage a relatively broad diet; as the costs of searching for preferred foods increase, they eventually overwhelm the economic advantage gained by being selective. A broad diet keeps search costs low even though it requires the forager to go after items that individually offer lower net yields. A second implication of the diet breadth model is that a resource in the optimal diet will always be pursued on encounter, since ignoring it inevitably reduces overall foraging efficiency. Because the chances of an encounter increase with density, each item in the optimal diet should contribute energy in proportion to its abundance in the forager’s habitat. Stationary resources such as mature seed-bearing grasses behave more like resource patches than mobile prey, but the implications for forager behavior are similar: frequent encounters result in frequent use. Therefore, a broad diet—one that accepts many different items as potential food—is not necessarily a highly diverse one (that is, both rich and equitable, in ecological terms). As Winterhalder and Goland (1997) have pointed out, even low-ranked resources such as small seeds can achieve considerable dietary importance if they occur in high densities. The diet breadth model shows in quantitative terms why and under what circumstances a broad diet can be more efficient than a narrow one, even though it entails exploitation of resources that have a relatively high cost : benefit ratio. Thus, it points to one path by which low-ranked plant resources attract the attention of human foragers. Once adopted, some of these plants benefited from exploitation in ways that increased their profitability and their dependability, further rewarding human management efforts and setting in motion the emergence of agricultural economies. We discuss three case studies that illustrate this application of the diet breadth model to understand the origins of food production. While all three cases argue for the transition to food production as an efficient strategy relative to foraging in the same environment—an economically rational response to changes in resource abundance in the environment—they differ in many particulars of timing and context. They also show how the diet breadth model can serve as a heuristic tool whether it succeeds or fails to predict the historical events known to archaeologists. In the lowland Neotropics, for example, the diet breadth model appears on the present evidence to effectively predict
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the emergence of food production between about 10,000 and 8,000 years ago (cal. BP). A robust and spatially large set of paleoecological data, now including those from tropical Mexico, indicates that food production was initiated within ecological contexts of rapid and significant changes of climate, vegetation, and fauna (e.g., transitions from savanna-like landscapes to tropical forest; replacement of megafauna by the smaller, fewer, and more dispersed tropical forest fauna). These changes appeared to have lowered the overall efficiency of foraging when the Ice Age ended, compared to foraging efficiency during the late- and terminal glacial periods (Piperno 2006; Piperno and Pearsall 1998). Judging from rates of foraging efficiency in modern hunters and gatherers from the tropics and elsewhere, environmental reconstructions, and archaeobotanical data, it appears that early food production in the Neotropics was probably a more efficient strategy than full-time hunting and gathering. The long-held notion that early farmers experienced diminishing returns to their labor should be reevaluated in all regions of the world, using robust measures of how costly it is to procure resources that were available to hunters and gatherers on the eve of food production and before. Declines in foraging efficiency can also result from resource depression (the depletion of prey populations under human predation; Charnov, Orians, and Hyatt 1976). In such cases, the diet breadth model lends rigor to the argument that human population density caused resource scarcity and therefore the adoption of wild cereals and other high-cost plant resources. While the diet breadth model provides a reasonably good fit with the pre-Neolithic “Broad Spectrum Revolution,” close examination of the archaeological record of subsistence change has yielded some important refinements in the way the model is typically applied by archaeologists. Stiner and colleagues (Stiner 2001; Stiner, Munro, and Surovell 2000) have pointed out that the fast-moving and expensive-to-catch animals added to later Paleolithic diets tended to have high reproductive rates and could therefore maintain relatively high densities even under predation pressure. Thus, the expansion of human diets not only served to maintain efficiency in the face of declining resource availability, as the diet breadth model predicts, but also simultaneously promoted reliance on sustainable resources. The Near East case suggests that the simplifying assumptions of the diet breadth model, while heuristically useful, are often at fault when its predictions fail. One such assumption is that immediate returns provide the best measure of utility. A resource that recovers rapidly under predation provides objectively superior yields over the long term compared to one that does not. Economists have noted that such delayed returns generally entail a subjective discounting of utility proportional to the uncertainty of the future reward (Tucker 2006). By the same logic, costs can likewise be devalued by time shifting. Subjective valuation of costs may shed some light on the apparent inefficiency of small seed crop cultivation in eastern North America. Assessed in terms of energy
Gremillion and Piperno Insights from the Emerging Evolutionary Synthesis
acquired per time spent, this strategy appears to have been highly inefficient, largely because of the high costs of processing small seeds. However, the high costs of processing seed crops once they are harvested should perhaps be evaluated in light of shifting time and energy preferences. Time spent winnowing, grinding, and cooking seeds would have been subjectively costly if it could have been spent more profitably doing something else—say, fishing or harvesting hickory nuts. However, during the winter and spring periods of food shortage in eastern North America, alternative activities were comparatively few. Seed processing in this context, while equally time consuming, was less costly than it would have been at harvest time (Gremillion 2004). Using present and future paleoecological and archaeological data, we should endeavor to study and identify on a greater geographical scale where diet breadth models are more effective and where they are less effective in predicting food production origins and dispersals. Where diet models are less effective, why is that the case, and what factors appear to better account for the beginnings of food production? Using examples such as the above from eastern North America, we should still ask whether diet breadth models potentially offer reasons why food production did not arise in eastern North America during the early and early-middle Holocene. For example, did ecological, demographic, and other factors of that period make nascent food production a less efficient strategy of food procurement than hunting and gathering?
Evo-Devo, Gene Expression, and Phenotypic (Developmental) Plasticity: Applications to Human Behavior and Agricultural Origins Recent research in the fields of developmental evolutionary biology (evo-devo) and phenotypic plasticity have complicated and enriched understanding of developmental pathways in plants and animals and the role they play in evolutionary change. A number of influential biologists have been moving away from older static models of the genetic code as blueprint and embracing newer ones that acknowledge a key role for gene expression and developmental plasticity in shaping phenotypes. For example, West-Eberhard (2003) argues that phenotypic plasticity often plays a leading role in evolutionary change by enabling the expression of variation upon which selection can act. In this view, novel phenotypes often arise from reorganizations of genomes, not by the spread or appearance of mutations, through changes in how existing genes are expressed (turned on and off) during the development of an organism. New phenotypic variation is rapidly introduced into populations without a corresponding genetic mutation. How does this happen? One mechanism is through an existing pool of genetic variation, called cryptic variation, that is unexpressed phenotypically or silent and thus hidden from natural selection (e.g.,
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Lauter and Doebley 2002). However, this hidden pool is environmentally plastic and can be set in motion by an environmental trigger, resulting in phenotypic variation. Genes called regulatory genes orchestrate this process by controlling gene expression. They are not standard protein-coding genes but rather act to switch other genes on or off or change when and where in an organism they are active (Kruglyak and Stern 2007; Orr 2005; Pigliucci 2005). Gene expression and phenotypic plasticity are now thought to be responsible for the origin of many novel traits (Kruglyak and Stern 2007; Orr 2005; Pigliucci 2005; West-Eberhard 2003). The new phenotypes generated by this process have the potential to become fixed (stabilized) by genetic assimilation if changed conditions are maintained over multiple generations. We can envision a number of ways in which the emerging synthesis of evolutionary biology and developmental biology can contribute to a better understanding of plant domestication. A common assumption is that crop evolution is driven by selection for rare mutants that are deleterious in wild plants or by selection for new random mutations that arose after cultivation began. It turns out, however, that in a number of major crops, some of these “domestication” genes are regulatory genes and that gene expression was involved in transformations of wild into domesticated phenotypes (e.g., Doebley 2006). It should be explored whether areas of genomes that were targeted by artificial selection possess considerable cryptic variation and plasticity that would have given rise to novel phenotypes in changing environments. Such environmental inductions of sufficient strength and stability to induce phenotypic plasticity and allow it to unfold were potentially of two major—and already well-documented—types: natural perturbations in climate and vegetation, which were uniquely profound and worldwide in scope at the origins of agriculture 12,000–10,000 years ago, and human habitat modification. Human selection of novel phenotypes in cultivated fields would lead to genetic accommodation (stabilization of the new genotypes). Phenotypic variants that have a selective advantage in environments that have undergone change as a result of natural or human alteration can therefore appear in a single generation by being environmentally induced from the existing pool of genetic variation.
Chenopodium and Maize: Possible Case Studies for Investigating Crop Plant Origins and Dispersals with Gene Expression Research Attention to phenotypic plasticity may help us to solve some persistent puzzles in the archaeological record of plant domestication. One such case is presented by Chenopodium berlandieri (goosefoot), a premaize domesticate of the eastern United States. In this species, the morphology of the prehistoric domesticated form is virtually identical to that of fruits found in small proportions of free-living, nondomesticated
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populations of the region. Anecdotal reports suggest that production of a majority of this alternative seed morph by individual plants is environmentally triggered (Asch and Asch 1977). Rapid induction of phenotypic change in goosefoot is consistent with the archaeobotanical record, which indicates considerable morphological variation but no directional trend in continuously variable traits such as seed size and seed coat thickness (Gremillion 1993). Maize’s ancestry and area of origin were contentious subjects for many years, no less so because of the fact that of all major crops, it least resembles its wild ancestor, Zea mays ssp. parviglumis (Balsas teosinte), in many important phenotypic characteristics (Doebley 2004). Teosinte and maize would seem to offer considerable opportunity for gene expression research. Molecular studies have shown that five to six regions of the Zea genome were involved in the transformation of teosinte into maize and that patterns of inheritance are complex and involved more than simple human selection on mutations that existed as rare variants in wild ancestral populations (Doebley 2004; West-Eberhard 2003, 265–269). Quantitative trait locus mapping of maize/teosinte hybrids by John Doebley’s (2004, 49) team suggests that “teosinte populations contain a pool of cryptic genetic variation upon which selection could have acted during maize domestication as proposed by Iltis.” With regard to specific maize domestication genes, tb1 is a major one that controls branching and inflorescence architecture in Zea. Teosinte is a bushy plant with many long, lateral branches that are tipped by tassels. Maize has shortened branches with a few large cobs occupying positions homologous to where teosinte tassels are located, and it has a solitary tassel located at the top of a single main branch. It is known that maizelike phenotypes in these characteristics can be directly induced by environmental stresses such as lowered temperatures and light intensity (West-Eberhard 2003). These conditions along with significantly lower ambient CO2 levels, another major stress factor, characterized late Pleistocene environments in Mexico (Piperno, Moreno, and Iriarte 2007). The question then becomes, did tb1 arise through an environmental induction or a mutation? In the former, human influence would have begun after nature and gene expression engineered this likely first major phenotypic step in maize evolution. Plants already maizelike in the characteristics that tb1 mediates would have been collected from the natural environment and grown in the first planting beds. The issue can be explored in part by experimentally growing teosinte under different kinds of environmental conditions and observing whether and to what degree sex transformation and associated changes in inflorescence characteristics are induced in the population. Researchers studying the processes of plant and animal domestication are in a position to understand how these newer ideas might shed new light on their own work. Zeder (2006) and Smith (2001) have both made the case that the emphasis among archaeobiologists on the morphological cri-
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teria for domestication is misplaced and that human behaviors implied by the archaeological record are of greater analytical and explanatory importance when it comes to understanding agricultural origins. Management and manipulation of natural resources can be powerful influences on the evolution of all the organisms involved even if the target species show no sign of altered morphology. This view is fully consistent with the evo-devo understanding of complex relationships between genotypes and highly plastic phenotypes. Likewise, organisms with plastic phenotypes respond to environmental variation in ways that can mimic the appearance and fixation of a simple mutation. The impact of environmental conditions on phenotypic expression is a topic that is also central to another theoretical innovation in biosciences, namely, the theory of niche construction. This theory proposes that the alteration of environmental conditions by organisms in ways that affect the outcome of selection in subsequent generations deserves to be regarded as a distinctive force of evolution alongside gene flow, genetic drift, mutation, and natural selection. While it remains to be seen whether the process of niche construction, which has long been recognized if not named by ecologists, merits elevation to such lofty status, we think that the concept has obvious relevance to the origins of agriculture. Coevolutionary theories already incorporate anthropogenic habitat modification as a key causal element in plant domestication. Simply keeping in mind the potential impacts of niche construction might change the way we think about long-term processes of change and could help in devising more realistic quantitative models of subsistence change.
Conclusions HBE represents a relatively new approach to understanding the evolutionary foundations of human behavior as expressed through extreme behavioral plasticity. In the face of criticisms both incisive and misguided, HBE has persisted in yielding insights into the origins of food production in numerous prehistoric populations. In contrast to the interest in human phenotypic adaptation displayed by HBE, phenotypic plasticity in plants has received little attention from anthropologists who study the origins of food production. However, we feel that it is time to move beyond the simplistic traditional view of plant domestication as a product of genetic mutations fixed by human intervention. A more complex and nuanced view of phenotype-genotype interactions is needed to complement and extend ecological and economic theories of plant domestication and agricultural origins. It is apparent that a new evolutionary synthesis will formally emerge in biology in the near future, incorporating fields such as evolutionary developmental biology (evo-devo). We should explore areas of potential intersection between HBE, dual inheritance models, and features of the new evolutionary synthesis in biology.
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