Reflections on nutrition in biological anthropology

Abstract

Some 50 years ago, and befittingly at an AAPA dinner, Stanley Garn delivered the Presidential Address, which he titled Nutrition in Physical Anthropology. In his address, Garn predicted, “a concern with nutrition in its broadest sense, including the physical form of the dietary and the energy balance will occupy us more rather than less in the years to come, as we channel our interests to ascertain the directions of evolutionary and physiological change…” (Garn, 1966). He specifically mentioned the nutritional underpinning of our interests in the evolution of the genus Homo, the diets of nonhuman primates, child growth, and sexual maturation, secular changes in adult body size, and growing evidence that obesity was replacing malnutrition in some populations. In this essay, we will take up Garn's prediction and review the themes related to human nutrition that occupy us in 2018. We define nutrition broadly: the consumption of food and the effect of food energy and nutrients on body size, health, and function. Nutrition is an area of interest shared with nutritional scientists and public health professionals, but the anthropological lens provides a view that is more comparative and evolutionary. As biological anthropologists, we are interested in the nutrition of a wide range of contemporary populations, as well as that of historic and prehistoric populations and the hominins in our evolutionary past. We consider nutrition as a key environmental factor in shaping human variability and evolution, and use the principles of evolution to explain variation between populations in the present as well as the past. We also recognize the inseparable nature of human cultural and biological adaptation to the environment, and hence use the explanatory frameworks referred to as biocultural or biobehavioral to address the biological-cultural nexus in studying nutrition. Three thematic areas have been prominent in the research of biological anthropologists in the past decade: diet in the evolution of the genus Homo, diet and nutrition in the transition from hunting and gathering to agriculture, and diet and nutrition in the current era of globalization. These thematic areas are defined by the time-period of interest and questions asked, but each is viewed as a transition in diet with measurable outcomes in terms of morphology and/or health. In the Paleolithic, major questions revolve around changes in the dietary niche of Homo, specifically the availability of dietary energy that enabled significant changes in the morphology (body size and brain size) observed. In the Neolithic, it is clear that the transition from foraging wild plant and animal species to the production of food via agriculture and animal husbandry changed the dietary niche in very significant ways. The timing and pace of this transition varied across geographic regions with the earliest dates at about 10,000 BCE. Questions of interest are related to how changes in nutritional ecology impacted body morphology and health in different geographical regions. In the current era, transitions in diet are associated with processes of industrialization and globalization that result in increases in food availability. Almost all human populations find themselves at some stage of this newest nutrition transition. Questions of interest revolve around the timing and pace of the transition in different populations, and the linkages between the changes in diet and the changes in body size, composition, and risk of chronic disease. Here we will consider each of the three thematic areas in turn. First, we will highlight major points in their historical development. Second, drawing on the research of biological anthropologists in the past decade, we will provide illustrative examples of each of these themes. We note, however, that given the interdisciplinary nature of current research, many people are associated with more than one area of research. We will finish with some thoughts on emerging trends. Biological anthropologists have had a longstanding interest in the diets of our ancestors. The enduring questions that capture our imaginations are: What did our ancestors eat? And, how did that diet shape the evolution of the genus Homo? These are important but difficult questions to answer. Important because an animal's diet is a key component of its adaptation to the environment. Difficult because ancestral populations lived long ago and walked the earth over a wide geographical range. We may never be able to answer these questions with the precision desired. As the subtitle of Ungar's (2007) book Evolution of the Human Diet so eloquently suggests, there are things we know, things we do not know, and things that are unknowable. Research over the past decade has addressed many questions and added significantly to what we do know (Ungar, 2007). Especially impressive are the gains in understanding of the diets of early hominins from the use of stable isotopes and dental microwear analysis (Ungar & Sponheimer, 2011). Here we focus on the diets of the genus Homo and two closely interrelated themes that have appeared in the literature in the past decade: (1) the nutritional qualities of foods in ancestral diets, and (2) models of Paleolithic diets in terms of categories of foods and nutrients and their relevance to modern health concerns. Interest in the nutritional qualities of foods in ancestral diets, specifically digestibility and nutrient composition, is driven by the classic question of how to explain the rapid expansion of brain and body size in early Homo, which are characteristics associated with an increase in diet quality. One of the first approaches was based on the concept of relative diet quality among primates, especially as it related to encephalization. Milton (1987) argued that the emergence of Homo was associated with a higher quality diet than that found in the other hominins. She based her claim on comparative gut anatomy and digestive kinetics in hominoids, arguing that gut proportions in humans were unusual and a derived condition indicative of a higher quality diet (e.g., a diet lower in fiber and lignin). She speculated that the incorporation of animal protein and animal fat into the diets of early humans was a key element in enabling them to maintain a high-quality diet while increasing body size, sociality, and levels of physical activity. Interestingly, Milton's idea of the importance of protein has prevailed, while the suggestion that animal fat was also important has largely disappeared. Leonard and Robertson (1992, 1994) approached the question of diet quality specifically in terms of energy needed to support the larger bodies and brains of early Homo. They argued that early Homo would have had a higher quality diet than that of nonhuman primates, and that the increase in quality would have come from meat consumption. Aiello and Wheeler's (1995) paper “The expensive tissue hypothesis” was a milestone because it provided such a clear link between metabolic energy needs for encephalization and morphology. They reasoned that since brain tissue has a high metabolic rate, a highly encephalized animal should have a higher than expected basal metabolic rate (BMR) for its body size; and since humans do not, something else had to have changed. They posited that a reduction in the size (and hence metabolic cost) of the gastrointestinal (GI) tract compensated exactly for the increased metabolic costs associated with a larger brain, and further that size reduction in the GI tract was made possible by the adoption of a higher quality diet, i.e. a diet lower in bulk (fiber) and higher in digestibility. The question of cooking is also about the role of diet quality in supporting encephalization in early Homo. More specifically, it is about improving the digestibility of foods to make dietary energy more available. Although it has long been recognized that cooking is unique to our genus and hence of evolutionary significance, there was little more than a general interest in the topic until the past couple of decades. Stahl's (1984) paper on plant food selection by early Homo is a notable exception. She argued that a nonfire using hominin would need to focus on plant foods high in soluble carbohydrates and low in starch because certain raw starches are relatively indigestible by modern humans. Aiello's and Wheeler's (1995) proposal that cooking was a way to externalize part of the digestion process and make it less metabolically expensive is also an exception. However, the actual effect of cooking on dietary energy availability received relatively little consideration until the work of Wrangham and colleagues (Carmody & Wrangham, 2009; Wrangham & Conklin-Brittain, 2003) focused attention on evidence for the beneficial effects of cooking on the net energy value of foods in human diets. Wrangham (2007, 2009, 2017) has argued for the significance of cooking in improving the digestibility, and hence energy value, in the diets of early Homo, specifically Homo erectus. Some evidence in support of this idea comes from experiments with a mouse model demonstrating that consuming cooked (oven roasted) versus raw tubers (sweet potatoes), oil seeds (peanuts), and meat (beef) resulted in improved body weight maintenance (Carmody et al., 2011; Groopman et al., 2014). Mice are not primates, and the sample sizes were extremely small, but their findings agree with research on contemporary humans demonstrating that cooking generally increases the digestibility of starchy foods (Wang & Copeland, 2013) and some nuts (Grundy et al., 2015); the research on cooked versus raw meats is inconclusive. Interestingly, the extent to which cooking affects starch gelatinization and hence improves digestibility is dependent on the amount of water used in cooking (Wang & Copeland, 2013), and it is likely that early Homo used dry roasting techniques. In another contribution to the question of cooking, Schnorr et al. (2015) demonstrated that modern day Hadza hunter-gatherers use a brief roasting technique that does not consistently improve in vitro enzymatic digestibility. This unexpected result complicates the story and indicates research is needed on a wide range of potential cooking techniques, and a wide range of potential foods. While living humans are not a perfect model for early Homo in terms of either dentition or gut anatomy and function, in vivo experiments would be useful. Further, the argument that modern humans cannot survive on a raw food diet (Wrangham, 2009, and elsewhere) needs better empirical support in terms of well-constructed dietary trials. It seems obvious that cooking food became important at some point in our evolutionary history and signaled a significant shift in the use of food resources. The unresolved question is when this occurred and how the process developed. Although Wrangham (2017) has consistently associated cooking with the morphological changes in early Homo that we interpret as linked to a higher quality diet, the archaeological evidence for the regular use of fire postdates those changes. Perhaps regular fire use was not linked to morphological changes in early Homo, but to later changes that left few morphological traces, or perhaps cooking did not increase energy availability as much as proposed. Colleagues in nutrition also argue that a high-quality diet was necessary to support the evolution of the large brain in Homo erectus, but they go further by proposing that aquatic foods would have been a necessary dietary component. This argument has focused largely on the biological need for docosahexaenoic acid (DHA), a long-chain polyunsaturated fatty acid predominant in neurological tissue (Brenna & Carlson, 2014). Although modern humans and nonhuman primates can synthesize DHA endogenously from shorter chain fatty acid precursors, synthesis is slow. Given that preformed DHA is more abundant in the marine food chain than the terrestrial, Cunnane and Crawford (2014) argue that the availability of marine resources was critical to encephalization. This is an interesting argument that challenges the disciplinary tendency in anthropology to focus on terrestrial resources in reconstructing the diets of early Homo, and Tattersall (2014) has argued that it is time to broaden the traditional focus and consider the role aquatic foods may have played. Data are limited, but it is clear that the DHA content of aquatic foods varies by species and by type of aquatic ecosystem, as might be expected (Joordens et al., 2014). It is also clear that the DHA content of anthropoid breastmilk varies with diet, and is higher in both human and nonhuman primate mothers who consume aquatic foods (Milligan & Bazinet, 2008). However, optimal dietary intakes of DHA for adults and infants are not known. Further, although it is clear that achieving species-typical brain size does require minimum levels of DHA, it does not follow that greater availability of DHA will lead to greater brain size. The second theme focuses on models of the diet of pre-agricultural Homo sapiens and relevance of these models to modern health concerns. The first model of a Paleolithic diet and claim that it was relevant to modern health concerns was Eaton and Konner's (1985) paper, “Paleolithic nutrition: A consideration of its nature and current implications.” The article, published in a respected medical journal, The New England Journal of Medicine, generated considerable interest, and critique, in both medical (Leaf & Weber, 1987) and anthropological communities (Garn & Leonard, 1989). It was the first in a series of papers arguing that we are genetically adapted to the characteristics of a Paleolithic diet—a diet based on minimally processed wild resources as compared to industrially processed foods—and that the changes in diet and lifestyle that began with the development of agriculture and animal husbandry have negatively affected our health. This basic argument has had considerable appeal beyond biological anthropology as numerous publications in medical and nutritional journals, as well as the popular press attest. Konner and Eaton (2010) recently updated their first paper on the “Paleolithic diet” (Eaton & Konner, 1985). Their basic argument in this and other contributions (Eaton et al., 2010) has remained essentially the same: (1) we are genetically adapted to the characteristics of Paleolithic diets; (2) changes in diet and lifestyle that began with the development of agriculture and animal husbandry some 10,000 years ago were too recent for us to have adjusted to genetically, and (3) our failure to adapt to new dietary conditions is responsible for current problems of chronic disease. The Paleolithic diet originally described (Eaton & Konner, 1985) was based largely on the diets of extant or historically known hunter-gatherer populations (Kung San, Hadza, Australian Aborigines, Inuit and Tasaday). Unfortunately, our understanding of these diets is constrained by the semi-quantitative and qualitative nature of most of the dietary intake data, which leads to uncertainty in quantitative estimates. It is also constrained by the limited eco-geographic and seasonal variation represented by the populations used. Acknowledging these limitations, the Paleolithic model demonstrates the broad pattern of nutrient intake on a diet based on naturally occurring food resources, and this broad pattern appears to be quite different from a diet based on modern industrialized foods. Ulijaszek, Mann, and Elton (2012) take a broader, deeper view of the evolution of the human diet in their book Evolving Human Nutrition: Implications for Public Health. They argue that the “natural” human diet was shaped across millions of years of evolutionary time before the Paleolithic period, and there is not, nor has there ever been, a “set” human diet. Rather, they argue that human nutritional history has been characterized by dietary diversity and flexibility, both of which were essential for coping with environmental seasonality and expansion into new geographic settings. As the book underscores, the human diet continues to evolve, and the authors’ goal is to bring an understanding of this evolving human diet to public health nutrition practices. Nutrition transitions are of interest because they alter the context in which humans live, presenting them with new suites of stressors, while relaxing others. On the broad scale, nutrition transitions are associated with changes in political, economic, and social structures. These, in turn, are associated with more proximal-level factors, such as diet (the focus of this discussion), activity patterns, demography, and disease exposure. Biological anthropologists have focused on understanding how these changing contexts influence human biological variation, especially in terms of health and morphology. The shifts in dietary patterns that accompanied the adoption of plant and animal domestication during the Neolithic have been a topic of considerable interest among biological anthropologists and the AJPA has and continues to serve as a key venue for these discussions. An enduring question that guides this research is: how did the transition to agriculture affect human health and morphology? A large body of literature published over the past 40–50 years indicates that dietary changes in the Neolithic negatively affected human health and were associated with reduced skeletal robusticity (Cohen & Armelagos, 1984; Larsen, 1995, 2006). Many recent studies continue to support earlier findings. For example, Mummert et al. (2011) conclude in their review that data published after Cohen and Armelagos (1984) generally confirm past research indicating plant and animal domestication had a negative impact on adult stature. Temple and Larsen (2007) found poorer oral health among agricultural versus hunter-gatherer groups in Japan. Data collected by May and Ruff (2016) on femoral morphology among Natufian hunter-gatherers and Neolithic farmers in the Levant support previous studies indicating a decline in skeletal robusticity with the transition to agriculture. And, Noback and Harvati (2015), in their analysis of 3D landmark datasets of crania from populations with known subsistence patterns, found some expected correlations between diet and cranial shape, but point out that the most significant differences were between populations dependent on plant- vs. animal-based diets, rather than between foragers and agriculturists. In the past decade, research on the transition to agriculture in the Neolithic has expanded into new geographic zones and researchers have increasingly adopted a biocultural approach in study design and data interpretation as advocated by Goodman and of the and data have biological anthropologists to new research questions including the that the foods associated with animal and plant domestication as shaping modern variation, both human and These have our understanding of the impact of dietary in the Neolithic on human health and morphology and in so are the We argue that the most important contributions of this recent are: (1) biocultural of and variation in health with plant and animal (2) use of stable isotopes to our understanding of variation in the pace and pattern of dietary across geographic and (3) evidence of human to foods. A of a biocultural interpretation is the work of and on the decline in oral health associated with the adoption of agriculture in Their analysis of variation, as well as of the of the them to that the increase in that accompanied the transition to agriculture, rather than dietary changes the dental patterns observed. As is associated with of the a higher rate would at increased risk of oral health, of changes in diet 2008). and (2010) also argue that other than diet for the changes in health with the transition to agriculture in the These studies a biocultural in that they

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