Social and Behavioral Epigenetics

AMERICAN ANTHROPOLOGIST

VITAL TOPICS FORUM Anthropological Genetics Andrew Kitchen, guest editor, and Amy L. Non, Clarence C. Gravlee, Connie J. Mulligan, Christina Warinner, Cecil M. Lewis Jr., Richard J. Bankoff, Heritiana D. D. Randrianatoandro, George H. Perry, Ripan S. Malhi, Alyssa C. Bader, and Jennifer Raff

DOI: 10.1111/aman.12364

INTRODUCTION: THE EXPANDING ROLE OF GENETIC INQUIRY IN ANTHROPOLOGY

Andrew Kitchen Department of Anthropology, University of Iowa, Iowa City, IA 52242; [email protected] Over the past few decades, anthropologists have increasingly used genetic approaches in their efforts to understand humans and their primate relatives. Technological and theoretical developments in recent years have enabled anthropological geneticists to expand their field of inquiry far beyond what was thought possible even a few years ago (Crawford 2000). Most importantly, the cost of collecting large genetic data sets has dropped dramatically, aiding researchers to better investigate complex questions such as the organization of our genome and the diversity of microbes living in our guts. Spectacular recent genetic discoveries, moreover, have altered understandings of our relationships to other hominin lineages. For example, genetic data have shown that both Neandertals (Green et al. 2010) and a newly discovered Denisovan population (Krause et al. 2010; Meyer et al. 2012) interbred with modern humans. Anthropological geneticists have long examined biological relationships among populations and described genetic variants such as disease-causing mutations that can be linked to specific human phenotypes (Crawford 2000). Great advances have been made on both fronts. The general patterns of human dispersal across the globe have been established (e.g., Henn et al. 2012). Genetic data continue to reveal the complex demographic histories of regional populations. In particular, studies have revealed how both geography and culture have stratified genetic diversity in contemporary populations. This can happen over short periods of time, as with the genetic stratification by religion of populations in the Levant (Haber et al. 2013). Our emerging understanding of diverse complex interactions between genetics and culture has both increased our understanding of these

topics and led researchers to investigate different kinds of problems. The essays in this forum describe some new lines of inquiry and practices of anthropological geneticists. Topics covered include health, ancient DNA, primate diversity, and education and outreach. The genetic component of human health continues to be a major focus of anthropological research. Amy Non and Clarence Gravlee discuss interactions between genetic ancestry, life experiences, and health. Researchers overly committed to genetic explanations of difference may underemphasize socioeconomic causes of health disparities; researchers overly committed to sociocultural explanations of differences may underemphasize the genetics of health. Non and Gravlee use examples to show how biocultural approaches combining genetics, economics, and culture are necessary to understand health disparities. Connie Mulligan looks at the health implications of epigenetics, a new field examining gene modifications that alter the production of proteins (gene expression) without changing the underlying DNA sequence of genes. Mulligan’s research in the Democratic Republic of the Congo examines how maternal stress during wartime affects the epigenetics of mothers and the health of their newborns. Microbes living on or in human bodies are a vital component of health. Christina Warinner and Cecil Lewis Jr. describe how microbes affect aspects of health such as weight and allergies. They point out that microbiomes evolve in response to changes in food-getting methods, sanitation, and diet. Researchers examining such changes in the past and present have increasingly emphasized the importance of collecting microbiome samples from non-Western subjects and ancient sources, such as fossilized dental plaque. Richard Bankoff, Heritiana Randrianatoandro, and George Perry explain how such ancient genetic data can provide critical information for ecologists attempting to conserve threatened or endangered primate species. Bankhoff, Randrianatoandro, and Perry also discuss difficult choices that researchers

C 2015 by the American Anthropological AMERICAN ANTHROPOLOGIST, Vol. 117, No. 4, pp. 736–749, ISSN 0002-7294, online ISSN 1548-1433.

Association. All rights reserved. DOI: 10.1111/aman.12364

Vital Topics Forum • Anthropological Genetics

collecting ancient DNA must make about funding priorities. Scientists attempting to make meaningful changes in the world must be able to explain their research results to nonspecialists. Anthropological geneticists, who often publish in technical journals and eschew popular writing, have not always made sufficient efforts to explain the practical utility of their work. Furthermore, the data-collection methods of anthropological geneticists may lead them to be regarded as neocolonialists exploiting the bodies of their “subjects.” This has caused problems for anthropological geneticists working among Native American populations in the continental United States. Ripan Mahli and Alyssa Bader discuss a summer workshop in which the participants are anthropological geneticists and Native Americans. The goal is for the two

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groups to have better understanding of one another’s concerns and to increase the agency of indigenous populations participating in genetic research. Finally, Jennifer Raff notes the paucity of forums in which research in anthropological genetics is explained to the general public. In her essay, Raff describes how she uses social media to explain the significance of such research. The essays here show that research in anthropological genetics requires holistic approaches to understanding the human condition. New findings in fields such as epigenetics are transforming our understanding of longstanding anthropological questions related to biological and cultural evolution. There seems little question that anthropological genetics will become an increasingly important part of our discipline in the near future.

Biology and Culture Beyond the Genome: Race, Racism, and Health Amy L. Non and Clarence C. Gravlee

DOI: 10.1111/aman.12365

Amy L. Non, Department of Anthropology, University of California, San Diego, La Jolla, CA 92093; [email protected]; http://www.amynon.org Clarence C. Gravlee, Department of Anthropology, University of Florida, Gainesville, FL 32611; [email protected]; http://gravlee.org; Twitter: @lancegravlee To what extent are health and disease shaped by genetic inheritance or by lived experience? Although it may sound like a medical question, it is fundamentally an anthropological one: it evokes old debates about nature and nurture and reminds us why cultural and biological anthropology sprang from the same discipline. As opposed to rehashing ideas from earlier centuries, current debate around genetic and environmental influences on health builds on recent discoveries about the complexity of disease and more nuanced understandings of the relations among genes, biology, and culture. However, these debates are also riddled with traps of reductionism and racial-genetic determinism. An integrative, anthropological approach that simultaneously leverages genetics and sociocultural data avoids these traps by recognizing (a) how culture shapes scientific interpretations of biological difference and (b) how systemic racism produces biological inequalities.

Historians and ethnographers have documented a legacy of scientific racism in U.S. medicine. In the antebellum South, African slaves who tried to escape slavery were labeled as mentally ill “drapetomaniacs.”1 This example is one of the earliest instances in the United States of racially motivated medicine in which the disease was designed to fit the needs of the white hegemony, with no basis in scientific evidence. Today similar logic pollutes modern biomedical research in subtle and pernicious ways. Researchers who begin with the assumption that race corresponds to intrinsic genetic differences observe disparities in biological outcomes—heart disease, cancer, or preterm birth, for example—and conclude that those disparities are genetic in origin. This circular reasoning reduces biology to genetics and reinforces the folk view that racial groups are distinct genetic categories. One manifestation of this logic is the narrow search for associations between DNA-based estimates of African genetic ancestry and phenotypes like obesity or high blood pressure. In one such study, Hua Tang and colleagues (2006) concluded that their results were “suggestive of genetic differences between Africans and non-Africans that influence blood pressure.” This assertion reflects a preconceived commitment to genetic explanations rather than evidence, as the study neither identified a statistically significant association with African ancestry nor tested alternative hypotheses. We

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American Anthropologist • Vol. 117, No. 4 • December 2015

reanalyzed the same dataset to examine how adding years of education—an admittedly crude but available measure of the social environment—affected associations between ancestry and blood pressure (Non et al. 2012). We found that increased education, but not genetic ancestry, predicted lower blood pressure in African Americans. Our finding is not surprising; the fact that so many studies continue to ignore environmental variables is. Our work in Puerto Rico further clarifies how sociocultural processes of racialization produce biological inequalities. Previous researchers had observed that darker skin color was associated with higher blood pressure in the African Diaspora. Some researchers saw the pattern as evidence of a racial-genetic predisposition to high blood pressure, while others suggested that darker-skinned people in colorconscious societies were more likely to experience social stressors related to blood pressure. The key to evaluating these alternative hypotheses was to distinguish between the cultural and biological dimensions of skin color. Clarence Gravlee, William Dressler, and H. Russell Bernard (2005) found that culturally ascribed color categories were associated with blood pressure differences, but skin pigmentation was not. We later found that culturally ascribed color status also predicted blood pressure better than did estimates of African genetic ancestry and that including sociocultural variables revealed genetic (but nonracial) associations that were otherwise hidden (Gravlee et al. 2009). Newer research is continuing to explore how sociocultural processes become biologically embedded along multiple pathways—from altering hormones to changing gene expression and even shortening our chromosomes. Epigenetics, a promising research area, is the study of molecular processes in which chemical modifications to the genome can alter the availability of genes to be transcribed into proteins. We and other researchers have been exploring epi-

genetic pathways through which sociocultural experiences such as early life adversity, trauma, or poverty affect health (Mulligan et al. 2012; Thayer and Non 2015). Among the Maori of New Zealand, for example, Zaneta Thayer has shown that pregnant mothers’ experience of racial discrimination, even more than poverty, is associated with epigenetic changes at stress-related genes and cortisol levels in their children (Thayer and Kuzawa 2015a, 2015b). This finding and the field of epigenetics more broadly add an important dimension to the debate around racial disparities in health because they draw attention to the intergenerational biological consequences of social inequalities. A priority for future research is to clarify the biological pathways through which sociocultural experiences can affect health. Epigenetics is a nascent field, and we are just beginning to determine where in the genome to look, what time periods in the lifespan are important, what tissues to target, and what social exposures really matter for health. In addition, we need improved methods for measuring the consequences of systemic racism in ways that can be connected to individual biological outcomes. In addition to more funding (always a concern), other needs include more training in genetics, rigorous statistical techniques for biological and cultural anthropologists alike, more training for medical students regarding human biological variation and the social construction of race, and increased incentives for collaboration across subdisciplines. Human biology is plastic and depends on the environment in which we develop and live. This is a lesson that Boas taught us a century ago, but it has been eclipsed by the more dominant gene-centered view of biology ever since. Now, as a more complex and dynamic view of biology begins to take hold, the time is right to reexamine exactly how entangled are human biology and culture.

Social and Behavioral Epigenetics Connie J. Mulligan

DOI: 10.1111/aman.12366

Connie J. Mulligan, Department of Anthropology, University of Florida, Gainesville, FL 32605, [email protected]; http://users.clas.ufl.edu/cmulligan/Webpage/index.html Epigenetic changes are chemical modifications in the genome that influence how DNA is used to make proteins that affect phenotypes but epigenetic changes do not alter DNA se-

quences. Most epigenetic alterations include the attachment of a simple chemical to DNA at certain sites (methylation) throughout the genome and modifications to the proteins that help package and organize DNA in chromosomes (Handel et al. 2009). These epigenetic alterations may play a role in transforming social, psychological, behavioral, or biological stressors into changes in the production of proteins (gene expression). From an evolutionary perspective, this would make sense. Epigenetic modification of protein


production may have evolved in higher-order organisms to provide short-term responses to changes in the environment without changing the underlying DNA sequence. In contrast, changes in DNA sequences occur infrequently over many generations and would provide long-term adaptations. My colleagues and I are conducting research in the Democratic Republic of Congo on the effects of maternal stress and war trauma on the methylation patterns of mothers and their newborns. This is an important question, as changes in methylation patterns may be associated with disease risk (Handel et al. 2009). We found that maternal war-related stress is associated with widespread (genomewide) changes in methylation patterns in the mothers but not in their newborns (Rodney and Mulligan 2014). We have also found that maternal war stress is associated with lower newborn birth weights (an indicator of maternal nutrition or stress) and changes in newborn methylation at specific genes (Mulligan et al. 2012). This is of special interest, as lower birth weights in newborns increase the risk of disease later in life. One particular gene whose methylation pattern in newborns is significantly correlated with maternal war stress is NR3C1 (Mulligan et al. 2012), which codes for a protein involved in newborn birth weight. The methylation pattern of the NR3C1 gene has also been shown to be altered in newborns of mothers experiencing depressed or anxious mood during the third trimester (Oberlander et al. 2008), suggesting that methylation of NR3C1 may play a key role in transferring the effects of environmental stress between generations. Our results suggest that stress may influence gene expression across a broad spectrum in the individual who directly experiences the stress—that is, the mother—whereas effects in the newborn may be focused on specific genes that are uniquely sensitive to environmental cues, such as NR3C1. It is interesting to note that war-stressed mothers and newborns do not share identical methylation patterns at NR3C1 (Mulligan et al. 2012). This suggests that methylation patterns at NR3C1 are not strictly inherited and may be more susceptible to environmental influences. This characteristic of the NR3C1 gene (and possibly other genes) may provide humans with an increased capacity for rapid change and adaptation to environmental stressors without producing long-lasting evolutionary change. Researchers have found there is an association between other forms of maternal stress, such as prenatal exposure to

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intimate partner violence (Radtke et al. 2011), and similar epigenetic alterations at the NR3C1 gene. This indicates that an array of violence-related maternal stressors may produce altered levels of methylation at NR3C1 in children. Altered methylation of the NR3C1 gene has also been linked to psychological trauma, including childhood abuse–related suicide (McGowan et al. 2009) and gender-specific post-traumatic stress disorder risk (Vukojevic et al. 2014). Methylation of NR3C1 is therefore a good example of intergenerational epigenetic effects, as multiple forms of maternal stress change methylation patterns of the NR3C1 gene. Social and behavioral epigenetics is a new field that is both emerging and still developing. Because social and behavioral epigenetics draws on concepts and data from anthropology, biology, medicine, psychology, and sociology, among others, the field is quintessentially interdisciplinary, as defined by the integration of multiple disciplines to create something new by crossing boundaries. Furthermore, the broad view of human health and disease that is embraced by social and behavioral epigenetics mirrors the comprehensive perspective on health and evolution that characterizes the field of anthropology. Finally, new molecular genetic technologies are generating more and larger epigenetic datasets for less money than ever before, enabling more investigators to initiate epigenetic studies regardless of their background. Much of the excitement surrounding this emerging field is driven by the hope that we may be able to address some of society’s most vexing problems, such as chronic social stressors and multigenerational cycles of violence, abuse, and poverty. Epigenetics has been studied for decades by molecular biologists who often focus on molecular mechanisms—that is, how methylation affects gene expression at a particular gene. More recently, social scientists have discovered that they can contribute a cultural, social, and behavioral dimension to epigenetic studies by looking at these effects on epigenetic changes at the individual or population level. Recently, a workshop on social and behavioral epigenetics was held with the goals of identifying critically important research questions needed to move the field forward as well as recognizing obstacles to addressing such questions.2 A report detailing the workshop recommendations on future research priorities in social and behavioral epigenetics can be found at http://www.nichd.nih.gov/about/meetings/ 2014/Documents/ExecSocialBehavEpigenetics_Sum.pdf.

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Microbiome and Health in Past and Present Human Populations Christina Warinner and Cecil M. Lewis Jr.

DOI: 10.1111/aman.12367

Christina Warinner, Department of Anthropology, University of Oklahoma, Norman, OK 73019; [email protected]; http://lmamr.org/ Cecil M. Lewis Jr., Department of Anthropology, University of Oklahoma, Norman, OK 73019; [email protected]; http://lmamr.org/ The human body contains approximately 100 trillion cells, of which more than 90 percent are microbial. These underexplored and mostly nameless microorganisms, collectively known as the human microbiome, weigh about as much as the human brain and harbor an immense diversity of genes that far exceed the functional capacity of our own genome, playing critical roles in digestion, vitamin production, drug metabolism, and immunity. This intimate relationship between humans and their microbes is being increasingly described by evolutionary biologists as that of a holobiont, a large interdependent and symbiotic community that evolves as a unit and cannot be understood by examining independent members alone (Zilber-Rosenberg and Rosenberg 2008). In part to address this reconceptualization of what it means to be human, the National Institutes of Health Common Fund launched the Human Microbiome Project (HMP) in 2007, an initiative whose goal was to better understand the human holobiont by sequencing all symbiotic microorganisms in and on the human body (Peterson et al. 2009). Over the past decade, high-throughput DNA and protein sequencing has opened up dramatic new opportunities to study the human microbiome; we now possess the tools necessary to comprehend and characterize the evolutionary ecology of the human microbiome and its role in health and disease. Numerous studies have revealed the complex and surprisingly central role the human microbiome plays in aspects of health as diverse as allergies and asthma risk (Gronlund et al. 2007; McLoughlin and Mills 2011), chemotherapy effectiveness (Karin et al. 2014), heart disease (Kholy et al. 2015), weight gain and loss (Angelakis et al. 2012), preterm labor risk (Witkin 2015), periodontal disease (Wang et al. 2013), and susceptibility to insect-borne infection (Verhulst et al. 2010). Moreover, microbiome

therapies have been shown to alleviate the symptoms of disorders and diseases such as antibiotic-associated colitis (Kassam et al. 2012) and rheumatoid arthritis (Ortiz et al. 2009). It is becoming increasingly clear that no study of human health or evolution is complete without consideration of our microbial self. Yet, while we have made great strides in revealing the diversity, variation, and evolution of the human genome, we know surprisingly little about the origins and diversity of the microbial portion of ourselves. Until very recently, nearly all studies of human evolution focused on the 10 percent of our cells and 0.7 percent of our genes that we conventionally call human. How has the other 90 percent of our cells and 99.3 percent of our hologenome evolved through time? Moreover, with few exceptions, even studies of the human microbiome have focused almost exclusively on Western industrialized societies, presenting a severe sampling bias that favors affluent metropolitan groups, potentially fostering downstream health disparities for under-represented peoples (Lewis et al. 2012). Anthropology can help remedy this. Much like traditional anthropological genetics, anthropological microbiome research will improve our understanding of human evolution and diversity. How did the primate gut evolve and adapt to climate and habitat changes? Were certain microbes passed down, mother to child, forming a unique aspect of heritability? What role did microbes and their diverse genetic functions play as hominins expanded into new continents and as humans transitioned from lowdensity bands of hunter-gatherers to dense urban-dwelling populations reliant on industrial agriculture and globalized supply chains? Addressing these questions not only expands our understanding of what it means to be human, but it also provides a much-needed foundation for improving the human condition. With the advent of industrialization, globalization, and modern sanitation, it is intuitive that we have changed our relationship with our own native microbiota, but we have little information about the ancestral state of our microbiome, and we therefore lack a foundation for characterizing this change and its impact on our health today. It has been persuasively argued that many of today’s socalled “diseases of civilization,” such as allergies, may be


exacerbated, if not caused, by recent changes in family size, living conditions, sanitation, diet, and antibiotics in industrialized nations, a concept known as the “hygiene hypothesis” (Strachan 1989). This hypothesis, which has been expanded to include the microbiome (Bendiks and Kopp 2013), posits that reduced microbial exposure and microbiome diversity early in life disrupts normal immune system development, leading to heightened predisposition to allergic diseases and autoimmune disorders. However, understanding how our industrialized lifestyle has affected our microbial health requires more precise knowledge of our preindustrial selves and the ancestral structure and function of our microbiome. An anthropological approach to the study of the human microbiome differs conceptually in important ways from research being conducted in the fields of medicine and microbiology, which primarily focus on clinical frameworks of disease risk and experimental manipulation of model microbial communities, respectively. Guided by biological anthropology’s traditional branches of primatology (nonhuman primates), paleoanthropology (extinct hominins), bioarchaeology (historic and prehistoric peoples), and human biology (diverse peoples today) and made possible by extraordinary technological advancements in molecular biology, investigations of the ancestral human microbiome are poised to make considerable contributions to evolutionary medicine and human health. The impact is already becoming apparent. The ancestral human microbiome appears to be characterized by a richer and more diverse array of microbes than those found in modern industrialized peoples. Primate studies have found evidence of rapid gut microbiome evolution in the human lineage (Moeller et al. 2014), where individual wild apes harbored a more diverse assortment of microbes than observed in humans today. Similarly, investigations of traditional hunter-gatherer societies have revealed major reductions in gut microbial diversity associated with the adoption of industrialized diets (Obregon-Tito et al. 2015; Schnorr et al. 2014). We found that among the microbes that have been lost is a multispecies clade of bacteria belonging to the genus Treponema (Obregon-Tito et al. 2015). These treponemes, which are found in nonhuman primates and which are common and relatively abundant in the gut microbiota of traditional peoples, irrespective of geography or diet, are puzzlingly absent in the guts of in-

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dustrial peoples. Although the exact roles and functions of these treponemes remain to be elucidated, partial genome reconstructions from metagenomic data and comparison to related taxa in animals suggest that they metabolize complex carbohydrates and produce short-chain fatty acids as waste products, a trait that in other microbial species is associated with anti-inflammatory properties (Fukuda et al. 2011; Hijova and Chmelarova 2007). It is thus tempting to hypothesize that the loss of these and other similar microbial species may be contributing factors in the rise of chronic inflammatory diseases, especially those originating in the gut. Much like the study of human genes, the study of microbiomes is not limited to extant traditional peoples and primates. Ancient samples, such as archaeological feces (coprolites), can provide valuable information about the ancient human gut microbiome (Tito et al. 2008), and indeed we have found that prehistoric feces contain treponemes and more closely resemble the gut microbiota of presentday traditional peoples than those in industrialized societies (Tito et al. 2012), again reinforcing the conclusion that the human-gut microbiome has undergone rapid and recent changes. Turning to the oral cavity, calcified dental plaque (calculus) provides direct access to ancestral oral microbiomes (Warinner et al. 2015b), and our discovery that it is the richest known source of ancient DNA in the archaeological record opens many doors for sophisticated analyses (Warinner et al. 2015a). Moreover, unlike coprolites, dental calculus is nearly ubiquitous and frequently abundant in skeletal assemblages, making detailed diachronic studies of ancestral oral microbiomes possible. Already, genetic and proteomic investigations of archaeological dental calculus have documented the presence of numerous periodontal and opportunistic pathogens in the oral cavities of historic and prehistoric populations (Warinner et al. 2014b), and they have even revealed dietary components that otherwise leave few traces (Warinner et al. 2014a; Warinner et al. 2014b). As such, coprolite and dental calculus studies are paving new paths to understanding the ancestral state of human biology and diet. The microbiome is a core component of our humanity. Anthropology has great potential to illuminate the long and intimate relationship between humans and their microbes and to lead to a deeper understanding of human health in the modern world.

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Primate Conservation Genomics and Paleogenomics Richard J. Bankoff, Heritiana D. D. Randrianatoandro, and George H. Perry

DOI: 10.1111/aman.12368

Richard J. Bankoff Department of Anthropology and Intercollege Program in Bioethics, Pennsylvania State University, University Park, PA 16802; [email protected] Heritiana D. D. Randrianatoandro Department of Anthropology, Pennsylvania State University, University Park, PA 16802, and Départment de Paléontologie et d’Anthropologie Biologique, Université d’Antananarivo, Madagascar; hdr11@ psu.edu; [email protected]; Twitter: @HeryRandry George H. Perry Departments of Anthropology and Biology, Pennsylvania State University, University Park, PA 16802; [email protected]; www.anthgenomicslab.com; Twitter: @grg_perry Conservation genomics has dual relevance to anthropology. At its core, the approach aims to inform efforts to preserve biodiversity and conserve threatened species. Species of concern include nonhuman primates, the subjects of much anthropological research. Additionally, conservation genomic inferences (from any organism) may be used indirectly to help reconstruct the history of anthropogenic impacts on the environment, thereby complementing the available archaeological and historical records. How can genomic data aid conservation efforts? If a goal is to maximally preserve taxonomic, genetic, phenotypic, and behavioral biodiversity, then genomic comparisons can help to establish conservation priorities by powerfully identifying cryptic species (true biological species not distinguishable based on external morphology), quantifying withinspecies population distinctiveness or genetic differentiation, and assessing levels of within-population genetic diversity across the range of a species, including the identification of inbreeding (Allendorf et al. 2010). Analyses of genomic differentiation across a landscape can also be used to determine which habitat-management regimes are best matched to territory sizes and dispersal patterns. Low genetic diversity is itself considered an extinction risk factor, because it negatively affects both disease resistance, with fewer pathogens recognized by the immune system, and long-term adaptability to ecological change, with less of the raw material (genetic variation) on which natural selection acts. Speculatively, genetic diversity may also serve as a proxy for yet undocumented phenotypic and behavioral variation. Finally, genomic data may also aid management practices for

captive populations of endangered species (Allendorf et al. 2010). With recent genomic method and sequencing technology advances, all of the above analyses can now be conducted with DNA extracted from noninvasive sources such as feces (Perry et al. 2010). This ability could facilitate sight-unseen sampling for genomic surveys—for example, from unhabituated groups—and obviate some undesirable or infeasible darting and trapping efforts (Arandjelovic et al. 2011; Perry 2014). These technological advances can likewise be extended to the large number of nonhuman primate skin and skeletal samples stored in museum collections worldwide (Burrell et al. 2015). When genomic data from museum samples of known spatiotemporal context are compared to those from current primate populations, the consequences of historical habitat loss, range contraction, hunting, and climate change on endangered populations can be quantified directly (Thalmann et al. 2011). In select cases, paleogenomic analyses of ancient DNA recovered from the subfossil remains of extinct primates or prehistoric populations of surviving taxa may provide information about extinction processes and risks that could inform future conservation efforts. For example, our group is using this approach to help advance understandings of how—in addition to body size—the extinct subfossil lemurs of Madagascar were similar or different to various surviving species. Reconstructed body masses for all 17 of the described extinct lemur species (11-160 kg; Jungers et al. 2008) are much larger than those of any extant lemur (the largest: 6.8 kg; Smith and Jungers 1997). We recently used paleogenomic methods to assemble complete or near-complete mtDNA genomes from five extinct lemur species and generate genetic diversity estimates from population samples for two of them, Palaeopropithecus ingens and Megaladapis edwardsi (Kistler et al. 2015). Comparisons with similar data from extant lemurs let us confidently resolve prior phylogenetic uncertainties and confirm that the extinct species did not represent a single clade (Godfrey 1988; Karanth et al. 2005; Kistler et al. 2015). Thus, taxonomic relationships should probably not be a primary concern when assessing future lemur extinction risk (see also Jernvall and Wright 1998). Meanwhile, genetic diversity estimates for P. ingens and M. edwardsi were lower than those for any of eight studied extant lemur species. This result is suggestive of lower historical population sizes for the large-bodied taxa, which


may have made these species especially susceptible to extinction in the face of habitat degradation and human hunting pressures (Kistler et al. 2015). We are now expanding our paleogenomic analyses to evaluate extinct lemur species definitions, test whether genetic diversity decreased following the arrival of humans to Madagascar, and advance reconstructions of extinct lemur behavioral ecology through analyses of nuclear genome sequence data. While genomic methods have great potential to elucidate thorny problems in primate conservation (e.g., Perry et al. 2013; Prado-Martinez et al. 2013; Xue et al. 2015), we would be remiss to not raise three issues for discussion. First, at a basic level we should consider how funds intended to effect the long-term viability of nonhuman primates are best invested among (a) direct species and habitat conservation efforts, (b) the collection and analysis of genomic data, and (c) economic development—all of which may help to ultimately achieve that goal. While DNA sequencing costs are steadily declining, genomic approaches are currently among the most expensive of anthropological research tools. Moreover, the bioinformatics toolkit required to adeptly analyze genomic data requires a substantial commitment in time, training, and computational resources. Second, for funds that are directed to conservation genomics, how

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should target species be selected—based on current conservation status, flagship potential, some measure of ability to mark ecosystem health, or another quality? For that matter, are primate-focused conservation genomic efforts less effective, ultimately even for our species of interest, than those that more fully consider the broader ecological community? Third, even with strong datasets it can be difficult to effectively and efficiently translate insights from conservation genomic analyses to meaningful conservation practice (Shafer et al. 2015). The challenges listed above are also opportunities to expand and enrich an interdisciplinary dialogue with concrete and urgently needed empirical recommendations for primate conservation genomic studies. In the end, great tools only matter in the context of well-defined questions and goals—and, in this case, appropriate follow-up changes to conservation practice. The work of integrating and translating data from any source into impactful results is intrinsically difficult; genomics is not unique or even exceptional in this regard. In the absence of broader evolutionary and ecological contexts, the tools of genomics are insufficient to advance the formulation of sound conservation policy; likewise, without genomic data, many other approaches alone may miss critical opportunities to effect meaningful change.

Engaging Native Americans in Genomics Research Ripan S. Malhi and Alyssa C. Bader

DOI: 10.1111/aman.12369

Ripan S. Malhi, Department of Anthropology and Carl R. Woese Institute for Genomic Biology, University of Illinois UrbanaChampaign, Urbana, IL 61801; [email protected] Alyssa C. Bader, Department of Anthropology, University of Illinois Urbana-Champaign, Urbana, IL 61801; acbader2@ illinois.edu Native North American groups have rarely been included in population-based genetic studies (Need and Goldstein 2009; Reich et al. 2012).3 The tumultuous history of interactions between scientists and the indigenous peoples of the Americas has likely contributed to the dearth of genomic data on Native North American peoples. For instance, researchers who have taken blood samples in indigenous communities have often not returned to report and explain research results (Wiwchar 2004). This exploitation of indigenous community members has created a mistrust of scientists (Schroeder et al. 2006) that leads many Native Americans to refuse to

participate in genetic studies. Genomic scientists have reacted to indigenous mistrust by using methods that favor statistical workarounds (Wall et al. 2011) or convenience sampling rather than making the necessary effort to develop strong collaborative relationships with indigenous communities. As a result, the little genetic data that have been collected from Native American communities have not been very informative. Overall, Native Americans have opted out or have been left out of major genomic efforts to understand human genetic diversity from populations worldwide such as the International HapMap Project and the 1000 Genomes Project. Genomic scientists have begun to engage in forms of community-based participatory research that involve mutually beneficial partnerships between scientists and Native Americans. An example of a large, successful partnership between genomic scientists and indigenous communities is the Northwest-Alaska Pharmacogenetics Research Network (NWA-PRGN; Woodahl et al. 2014). This partnership, which conducts basic and applied pharmacogenomics

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research, includes both indigenous and nonindigenous institutions throughout North America.4 There are also numerous smaller-scale partnerships on genomic studies. Protocols that help develop trust and clearly define expectations for all stakeholders are particularly vital in these smaller partnerships (Malhi 2009). For example, formalized research agreements between scientists and indigenous communities, as well as timely meetings, allow the expectations for each partner to be defined and, if necessary, modified. The National Congress of American Indians (NCAI), with support from the National Human Genome Research Institute (NHGRI), has created an online Genetics Resource Center with templates and models of research agreements between scientists and indigenous communities that can be used to help initiate these partnerships. Most genomic scientists are of European descent and lack detailed knowledge of the histories, cultures, and sociopolitical concerns of indigenous peoples. Indigenous scientists may be more likely to anticipate, recognize, and navigate potentially delicate social and political issues that arise in projects with indigenous peoples as participants (McInnes et al. 2011). There are now training and internship programs that aim at both increasing the number of indigenous genomic scientists and the general knowledge of the field of genomics in indigenous communities. In 1998, GENA (Genetic Education for Native Americans) began offering workshops on genetics at national conferences. Since 2011, we have been participating in the SING (Summer Internship for Native Americans in Genomics) program of one-week workshops aimed at facilitating discussions between indigenous students and genomic researchers, dissolving barriers between in-

digenous communities and scientists, and providing students with access to active researchers in the field. Because most scientific research is rooted in Western thought, we examine how genomic tools can complement indigenous forms of knowledge in ways that serve Native American interests. We discuss, for example, how indigenous communities can use genomics to aid in the stewardship of nature, improvements in the health of community members, and legal claims of land and ancestral remains. Combining ethical, legal, and social discussions surrounding historical Native American encounters with science and hands-on training in the latest genomics techniques and analytical programs, the SING workshop helps prepare participants for future leadership positions in science, research, and teaching careers. Beyond the academic training component, programs like SING help to foster networks for Native students to explore potential research interests and voice concerns in a socially supportive space. Developing and maintaining mutually beneficial partnerships is an important step in improving the quality of genomic studies. Such research requires appropriate and ethical sampling, which cannot be accomplished without mutual respect between indigenous communities and scientists. Training and supporting indigenous scientists to be leaders in their fields increases indigenous community knowledge about genomic research and diversifies scientific research perspectives. Community partnerships also require scientists to personally engage with populations of interest, contributing to a stronger, more nuanced understanding of the social context of research questions. The creation of such diverse research teams will lead to better genomic science (Paige 2008).

Anthropological Genetics and Social Media Jennifer Raff

DOI: 10.1111/aman.12370

Jennifer Raff Department of Anthropology, University of Kansas, Lawrence, KS 66045; [email protected]; https:// about.me/jenniferraff; Twitter: @jenniferraff Anthropological geneticists should participate in public engagement because of the complexity of their work, its implications for human health and societies, and its tendency to be co-opted for particular political or social agendas. They are positioned to offer important contributions to public conversations on issues of race, genetic identity, history, and conflict. There are multiple avenues to public outreach

for academics; among them, social media is a powerful, underused tool. Social media networks allow the circumvention of traditional communication barriers between scientists and the general public. One example is the response of the anthropological genetics community to the publication of Nicholas Wade’s (2014) book, A Troublesome Inheritance. Wade argued that “racial” differences related to genetic variation could explain socioeconomic disparities and cultural characteristics. The American Anthropological Association responded quickly by hosting a web debate between Agust´ın Fuentes and Wade. I wrote a review of Wade’s book on my blog, Violent Metaphors (http://tinyurl.com/raffwadereview), and


participated in several back-and-forth exchanges with Wade, Fuentes, and Jon Marks on the Huffington Post and other sites.5 I also joined a discussion analyzing Wade’s book with New York Times reporter David Dobbs on the podcast “Science for the People.” Other academics wrote online reviews, and a group of prominent geneticists published a letter in the New York Times denouncing Wade’s methodology and conclusions. The book was discussed extensively on Twitter, and the official journal of the American Association of Anthropological Genetics, Human Biology, published a special open-access issue (Vol. 86, no. 3) that included many of the online reviews of the book. This public conversation was an excellent illustration of how anthropologists can make complex topics accessible for broad audiences. (At the time of writing this piece, my review has been accessed 18,790 times on my website, far more than any of my research papers). Social media is also an effective means of disseminating basic scientific information on the Internet. I recently searched for terms related to human evolution; dismayingly, the top results were from the creationist website Answers in Genesis. By using social media to confront such pseudoscience and to distribute accurate information, anthropological geneticists can have a significant effect on public scientific literacy. Furthermore, social media can enhance engagement between researchers and the communities with which they work by improving accessibility to project information and researchers. In our work with North Slope Alaskan communities, we have observed that younger project participants are reached more easily through social media than in person (and that they are more likely to share information about the research with others in the community if it is online). Our research group therefore maintains a website that disseminates information and offers community members an easy way to reach us with feedback and questions. Other researchers use Facebook groups, project blogs, Twitter lists, and e-mail discussion lists to stay in contact with project participants and colleagues. By writing about genetics research in a way that is accessible for general audiences, anthropological geneticists can also increase the visibility of our subdiscipline. This is a particular concern for anthropological genetics because it is a small and relatively young field. Ask a member of the public what an anthropological geneticist does, and you are more likely to get a blank stare in response than if you ask about what an archaeologist does. By using social media, anthropological geneticists can improve public understanding of who they are and what they study. Journalists seeking comments on stories pay attention to our social media presence. I have been consulted on breaking science news on multiple occasions because journalists have seen what I have written on Twitter, on the Huffington Post, and on my blog. I was recently interviewed by journalists from Nature News, Associated Press, and the New York Times seeking my comments on a high-profile article analyzing the Kennewick Man genome. Because the journal allowed just a 24-hour embargo, science

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reporters were scrambling to find sources that could quickly read the article and comment. Journalists contacted me because I had written on social media about Native American paleogenomics, the early peopling of the Americas, and the need for decolonizing Native American genomics. One place to start social media outreach is at the department level, through group blogs or accounts contributed to by multiple faculty members. Excellent examples are the Debunking Genetic Astrology page run by genetics faculty at University College London (https:// www.ucl.ac.uk/mace-lab/debunking) and the Learn Genetics pages by The Genetic Science Learning Center at The University of Utah (http://learn.genetics.utah.edu/). Another simple approach is to add a blog or forum to one’s lab webpage to which all members contribute. This gives lab members the opportunity to practice writing for the public, enhances students’ and postdocs’ professional visibility, and allows labs to showcase their research. Individual outreach efforts beyond that can take many forms, such as podcasting, long-form writing, Instagram, Twitter, Tumblr, Facebook, and video blogs, depending on one’s goals. For example, during the publication of our most recent article, our research group worked with several science writers to translate and disseminate the findings in several different online publications with a broad public readership. As an early career researcher, using social media to expand the readership of my work has helped me develop relationships with many more people in my field, science writers, and interested members of the public than would otherwise have been possible. It has also allowed me to make a larger contribution to the field than I would have been able to do in the absence of social media. But there have been downsides. When I have written about controversial issues such as race and genetics, I have attracted unwelcome attention from people who vehemently disagree with me. Although these individuals vary in their degree of commitment and vitriol, the broader conversation has always included a heavy dose of misogynistic commentary (and on rare occasions threats to my career or physical safety). While such misogyny is a near-universal experience of women of all levels of seniority who write publicly, direct and indirect threats to careers are particularly worrisome for junior academics engaged in social media outreach. An additional concern for early-career stage academics is the time it takes to blog, tweet, and do media interviews. Nevertheless, social media outreach is a form of teaching and, as such, should be valued by academics. I urge more anthropological geneticists at all stages of their careers to consider expanding their use of social media. NOTES

1. Drapetomania was defined by Dr. Samuel Cartwright in the 1850s as a mental illness that caused slaves to run away. It is now understood as an example of scientific racism.

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2. Workshop on Social and Behavioral Epigenetics, held on July 29–30, 2014, in Potomac, Maryland, and supported by the NSF (BCS-1448213; BCS-1231264), Eunice Kennedy Shriver National Institute of Child Health and Human Development, UK Science and Innovation Network, Economic and Social Research Council (ESRC), Biotechnology and Biological Sciences Research Council (BBSRC), and Research Councils UK (RCUK). 3. NHGRI-EBI GWAS (Genome Wide Association Studies) Catalog. 4. Applied research to use biomedical data to develop drugs and appropriate dosage for patients. 5. These responses may be found at the following web addresses: http://tinyurl.com/raffwadecritique, http: //tinyurl.com/fuenteswadecritique, http://tinyurl. com/markswadecritique, http://tinyurl.com/wade responsetocrtics, http://tinyurl.com/raffwaderespo nse, http://tinyurl.com/fuenteswaderejoiner, http: //tinyurl.com/markswaderesponse.

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