Keith Hunley

The global pattern of gene identity variation reveals a history of long‐range migrations, bottlenecks, and local mate exchange: Implications for biological race

Several recent studies have argued that human genetic variation conforms to a model of isolation by distance, whereas others see a predominant role for long-range migrations and bottlenecks. It is unclear whether either of these views fully describes the global pattern of human genetic variation. In this article, we use a coalescent-based simulation approach to compare the pattern of neutral genetic variation predicted by these views to the observed pattern estimated from neutral autosomal microsatellites assayed in 1,032 individuals from 53 globally-distributed populations. We find that neither view predicts every aspect of the observed pattern of variation on its own, but that a combination of the two does. Specifically, we demonstrate that the observed pattern of global gene identity variation is consistent with a history of serial population fissions, bottlenecks and long-range migrations associated with the peopling of major geographic regions, and gene flow between local populations. This history has produced a nested pattern of genetic structure that is inconsistent with the existence of independently evolving biological races. We consider the implications of our findings for methods that apportion variation into within- and between-group components and for medical genetics.

Genetic and Linguistic Coevolution in Northern Island Melanesia

Recent studies have detailed a remarkable degree of genetic and linguistic diversity in Northern Island Melanesia. Here we utilize that diversity to examine two models of genetic and linguistic coevolution. The first model predicts that genetic and linguistic correspondences formed following population splits and isolation at the time of early range expansions into the region. The second is analogous to the genetic model of isolation by distance, and it predicts that genetic and linguistic correspondences formed through continuing genetic and linguistic exchange between neighboring populations. We tested the predictions of the two models by comparing observed and simulated patterns of genetic variation, genetic and linguistic trees, and matrices of genetic, linguistic, and geographic distances. The data consist of 751 autosomal microsatellites and 108 structural linguistic features collected from 33 Northern Island Melanesian populations. The results of the tests indicate that linguistic and genetic exchange have erased any evidence of a splitting and isolation process that might have occurred early in the settlement history of the region. The correlation patterns are also inconsistent with the predictions of the isolation by distance coevolutionary process in the larger Northern Island Melanesian region, but there is strong evidence for the process in the rugged interior of the largest island in the region (New Britain). There we found some of the strongest recorded correlations between genetic, linguistic, and geographic distances. We also found that, throughout the region, linguistic features have generally been less likely to diffuse across population boundaries than genes. The results from our study, based on exceptionally fine-grained data, show that local genetic and linguistic exchange are likely to obscure evidence of the early history of a region, and that language barriers do not particularly hinder genetic exchange. In contrast, global patterns may emphasize more ancient demographic events, including population splits associated with the early colonization of major world regions.

Race reconciled?: How biological anthropologists view human variation

Maxwell Museum of Anthropology, University of New Mexico, Albuquerque, NM 87131In May 2006, the authors of this introduction had anargument about how best to describe and interprethuman biological variation. The disagreement focused onwhether human races exist, and, even if they do,whether we should continue to use the term ‘‘race’’ inour research and teaching. We eventually realized thatwe were re-hashing an argument that has no doubttaken place for generations (e.g., Mason, 1960; Montagu,1964; Mead et al., 1968; also see Anthropology Newslet-ter 1997-1998 and Caspari, this issue) and that our dif-ferent training, research interests, and life experienceshad led us to approach the study of human biologicalvariation from very different perspectives. One of us is agenetic anthropologist interested in the global pattern ofneutral genetic variation. The other is a bioarchaeologistinterested in how patterns of phenotypic variation areshaped by culture in the United States. Our exchange,coupled with our reading of recent literature from vari-ous subfields of biological anthropology, led us to suspectthat our inability to communicate is widespread withinour discipline and that it hampers effective collaboration.Inadequate communication and collaboration likely leadto less than optimum progress in solving important an-thropological problems and send conflicting signals abouthuman variation to our students and the public.To address these issues, we decided to organize ameeting of scholars who had made original and impor-tant contributions to the study of human variation. Thepurpose of the meeting would be to outline our differen-ces, to determine if they could be reconciled, and toexplore ways to more effectively communicate our heter-ogeneous views within and outside our various disci-plines.In May 2007, the Maxwell Museum and Departmentof Anthropology of the University of New Mexico hosteda symposium entitled, ‘‘Race Reconciled?: How BiologicalAnthropologists View Human Variation.’’ The symposiumwas attended by scholars who specialize in human biol-ogy, genetics, forensics, bioarchaeology, and paleoanthro-pology and who hold a wide spectrum of views about thenature, causes, and social and scientific implications ofpatterns of human biological variation. We had two spe-cific goals. The first was to communicate to one anotherour diverse views of human biological variation and thedata and methods we use to arrive at those views. Par-ticipants were asked to give 40-min lectures thataddressed the following questions:What is race? What is the relationship between yourdefinition of race and your view of the structure ofhuman biological variation? What specific data andmethods did you employ to reach this view? What arethe implications of your view for understanding one ormore of the following?human originshuman population history the relationship between human biology, language,and culture the genetic and environmental components of complexdisease forensic identification whether or how to use the term ‘‘race’’ in research andteachingThe second goal of the symposium was to identify com-mon ground and significant points of disagreement, andto determine how disagreements should be discussedwithin our discipline and communicated to the largerscientific community, to our students, and to the public.To achieve this goal, the participants were asked to con-sider the following questions:Can we reconcile our disparate views of biological vari-ation? If so, how? If not, how do we effectively (1) stimu-late communication and collaboration within anthropol-ogy and the larger academic community, and (2) commu-nicate our different views to our students and to thepublic in ways that make the points of agreement anddisagreement and their broader implications clear?

The impact of founder effects, gene flow, and European admixture on native American genetic diversity.

Recent studies have concluded that the global pattern of neutral genetic diversity in humans reflects a series of founder effects and population movements associated with our recent expansion out of Africa. In contrast, regional studies tend to emphasize the significance of more complex patterns of colonization, gene flow, and secondary population movements in shaping patterns of diversity. Our objective in this study is to examine how founder effects, gene flow, and European admixture have molded patterns of neutral genetic diversity in the Americas. Our strategy is to test the fit of a serial founder effects process to the pattern of neutral autosomal genetic variation and to examine the contribution of gene flow and European admixture to departures from fit. The genetic data consist of 678 autosomal microsatellite loci assayed by Wang and colleagues in 530 individuals in 29 widely distributed Native American populations. We find that previous evidence for serial founder effects in the Americas may be driven in part by high levels of European admixture in northern North America, intermediate levels in Central America, and low levels in eastern South America. Geographically patterned admixture may also account for previously reported genetic differences between Andean and Amazonian groups. Though admixture has obscured the precise details of precontact evolutionary processes, we find that genetic diversity is still largely hierarchically structured and that gene flow between neighboring groups has had surprisingly little impact on macrogeographic patterns of genetic diversity in the Americas.

Rejection of a serial founder effects model of genetic and linguistic coevolution

Recent genetic studies attribute the negative correlation between population genetic diversity and distance from Africa to a serial founder effects (SFE) evolutionary process. A recent linguistic study concluded that a similar decay in phoneme inventories in human languages was also the product of the SFE process. However, the SFE process makes additional predictions for patterns of neutral genetic diversity, both within and between groups, that have not yet been tested on phonemic data. In this study, we describe these predictions and test them on linguistic and genetic samples. The linguistic sample consists of 725 widespread languages, which together contain 908 distinct phonemes. The genetic sample consists of 614 autosomal microsatellite loci in 100 widespread populations. All aspects of the genetic pattern are consistent with the predictions of SFE. In contrast, most of the predictions of SFE are violated for the phonemic data. We show that phoneme inventories provide information about recent contacts between languages. However, because phonemes change rapidly, they cannot provide information about more ancient evolutionary processes.

Does Lateral Transmission Obscure Inheritance in Hunter-Gatherer Languages?

In recent years, linguists have begun to increasingly rely on quantitative phylogenetic approaches to examine language evolution. Some linguists have questioned the suitability of phylogenetic approaches on the grounds that linguistic evolution is largely reticulate due to extensive lateral transmission, or borrowing, among languages. The problem may be particularly pronounced in hunter-gatherer languages, where the conventional wisdom among many linguists is that lexical borrowing rates are so high that tree building approaches cannot provide meaningful insights into evolutionary processes. However, this claim has never been systematically evaluated, in large part because suitable data were unavailable. In addition, little is known about the subsistence, demographic, ecological, and social factors that might mediate variation in rates of borrowing among languages. Here, we evaluate these claims with a large sample of hunter-gatherer languages from three regions around the world. In this study, a list of 204 basic vocabulary items was collected for 122 hunter-gatherer and small-scale cultivator languages from three ecologically diverse case study areas: northern Australia, northwest Amazonia, and California and the Great Basin. Words were rigorously coded for etymological (inheritance) status, and loan rates were calculated. Loan rate variability was examined with respect to language area, subsistence mode, and population size, density, and mobility; these results were then compared to the sample of 41 primarily agriculturalist languages in [1]. Though loan levels varied both within and among regions, they were generally low in all regions (mean 5.06%, median 2.49%, and SD 7.56), despite substantial demographic, ecological, and social variation. Amazonian levels were uniformly very low, with no language exhibiting more than 4%. Rates were low but more variable in the other two study regions, in part because of several outlier languages where rates of borrowing were especially high. High mobility, prestige asymmetries, and language shift may contribute to the high rates in these outliers. No support was found for claims that hunter-gatherer languages borrow more than agriculturalist languages. These results debunk the myth of high borrowing in hunter-gatherer languages and suggest that the evolution of these languages is governed by the same type of rules as those operating in large-scale agriculturalist speech communities. The results also show that local factors are likely to be more critical than general processes in determining high (or low) loan rates.

The apportionment of human diversity revisited.

OBJECTIVES Studies of the apportionment of human genetic diversity have found that local populations harbor nearly as much diversity as the species as a whole. These studies have been a valuable cornerstone in rejecting race as a biological framework in anthropology. The current study presents new analyses that use updated statistical methods based on bifurcating trees to assess the structure of human genetic diversity and its implications for the existence of canonical biological races. MATERIALS AND METHODS We examine patterns of both goodness-of-fit and lack-of-fit of two bifurcating trees to patterns of diversity determined from autosomal short tandem repeat genotypes in 1,037 people representing 52 populations with worldwide distribution. RESULTS From goodness-of-fit, we infer a root for the tree within Africa, and we recapitulate a pattern of decreasing genetic diversity with increasing geographic distance from Africa. From lack-of-fit, we present tentative evidence for admixture events with archaic hominins. We do not find evidence that long-range migration or local gene flow have contributed appreciably to the lack of fit at a global scale. CONCLUSION This is the first study to find a root for a tree of human populations without comparison to a nonhuman out-group, and it is one of the first studies to identify a signature of admixture with archaic hominins without reference to ancient DNA. Our findings complement previous studies of the apportionment of human diversity and provide a more solid evolutionary foundation for the rejection of biological race. Am J Phys Anthropol 160:561-569, 2016.

The effects of socioeconomic status, clinical factors, and genetic ancestry on pulmonary tuberculosis disease in northeastern Mexico.

Diverse socioeconomic and clinical factors influence susceptibility to tuberculosis (TB) disease in Mexico. The role of genetic factors, particularly those that differ between the parental groups that admixed in Mexico, is unclear. The objectives of this study are to identify the socioeconomic and clinical predictors of the transition from latent TB infection (LTBI) to pulmonary TB disease in an urban population in northeastern Mexico, and to examine whether genetic ancestry plays an independent role in this transition. We recruited 97 pulmonary TB disease patients and 97 LTBI individuals from a public hospital in Monterrey, Nuevo León. Socioeconomic and clinical variables were collected from interviews and medical records, and genetic ancestry was estimated for a subset of 142 study participants from 291,917 single nucleotide polymorphisms (SNPs). We examined crude associations between the variables and TB disease status. Significant predictors from crude association tests were analyzed using multivariable logistic regression. We also compared genetic ancestry between LTBI individuals and TB disease patients at 1,314 SNPs in 273 genes from the TB biosystem in the NCBI BioSystems database. In crude association tests, 12 socioeconomic and clinical variables were associated with TB disease. Multivariable logistic regression analyses indicated that marital status, diabetes, and smoking were independently associated with TB status. Genetic ancestry was not associated with TB disease in either crude or multivariable analyses. Separate analyses showed that LTBI individuals recruited from hospital staff had significantly higher European genetic ancestry than LTBI individuals recruited from the clinics and waiting rooms. Genetic ancestry differed between individuals with LTBI and TB disease at SNPs located in two genes in the TB biosystem. These results indicate that Monterrey may be structured with respect to genetic ancestry, and that genetic differences in TB susceptibility in parental populations may contribute to variation in disease susceptibility in the region.

Reassessment of global gene–language coevolution

In On the Origin of Species, Darwin proposed that human races and languages evolved in concert following a tree-like history of splits and isolation (1). Linguists and anthropologists have long been skeptical of this idea because historical and ethnographic evidence suggest that group boundaries are fluid and differentially permeable to the movement of peoples and languages. For this reason, as Sapir (2) so eloquently put it, “the history of each is apt to follow a distinctive course.” In PNAS, Creanza et al. (3) weigh in on this debate and provide a conceptual and methodological framework for future studies of population genetic and linguistic coevolution.

Social-group identity and population substructure in admixed populations in New Mexico and Latin America

We examined the relationship between continental-level genetic ancestry and racial and ethnic identity in an admixed population in New Mexico with the goal of increasing our understanding of how racial and ethnic identity influence genetic substructure in admixed populations. Our sample consists of 98 New Mexicans who self-identified as Hispanic or Latino (NM-HL) and who further categorized themselves by race and ethnic subgroup membership. The genetic data consist of 270 newly-published autosomal microsatellites from the NM-HL sample and previously published data from 57 globally distributed populations, including 13 admixed samples from Central and South America. For these data, we 1) summarized the major axes of genetic variation using principal component analyses, 2) performed tests of Hardy Weinberg equilibrium, 3) compared empirical genetic ancestry distributions to those predicted under a model of admixture that lacked substructure, 4) tested the hypotheses that individuals in each sample had 100%, 0%, and the sample-mean percentage of African, European, and Native American ancestry. We found that most NM-HL identify themselves and their parents as belonging to one of two groups, conforming to a region-specific narrative that distinguishes recent immigrants from Mexico from individuals whose families have resided in New Mexico for generations and who emphasize their Spanish heritage. The “Spanish” group had significantly lower Native American ancestry and higher European ancestry than the “Mexican” group. Positive FIS values, PCA plots, and heterogeneous ancestry distributions suggest that most Central and South America admixed samples also contain substructure, and that this substructure may be related to variation in social identity. Genetic substructure appears to be common in admixed populations in the Americas and may confound attempts to identify disease-causing genes and to understand the social causes of variation in health outcomes and social inequality.