Toward a New History and Geography of Human Genes
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Feature Review Toward a new history and geography of human genes informed by ancient DNA 1,2 3,4,5 Joseph K. Pickrell and David Reich 1 New York Genome Center, New York, NY, USA 2 Department of Biological Sciences, Columbia University, New York, NY, USA 3 Department of Genetics, Harvard Medical School, Boston, MA, USA 4 Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA 5 Broad Institute of the Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, MA, USA Genetic information contains a record of the history of which propose that the present-day inhabitants of a region our species, and technological advances have trans- descend from people who arrived during periods of tech- formed our ability to access this record. Many studies nological or cultural change, replacing the previous inha- have used genome-wide data from populations today to bitants. learn about the peopling of the globe and subsequent In archaeology, this debate has played out around the adaptation to local conditions. Implicit in this research is issue of whether sudden changes in material culture ap- the assumption that the geographic locations of people parent in the archaeological record can be attributed to the today are informative about the geographic locations of spread of culture or to population movements: ‘pots versus their ancestors in the distant past. However, it is now people’ [1]. In physical anthropology, the debate has played clear that long-range migration, admixture, and popula- out around the issue of whether changes in morphological tion replacement subsequent to the initial out-of-Africa characters over time are due to in situ evolution or to the expansion have altered the genetic structure of most of arrival of new populations (e.g., [2]). the world’s human populations. In light of this we argue The same debate has also played out in genetics. On the that it is time to critically reevaluate current models of side of population replacements, there are the ‘wave of the peopling of the globe, as well as the importance of advance’ and ‘demic diffusion’ models, first proposed to natural selection in determining the geographic distri- describe the spread of agriculture through Europe. In these bution of phenotypes. We specifically highlight the models, the Neolithic transition was accompanied by the transformative potential of ancient DNA. By accessing spread of farmers from the Near East across Europe, who the genetic make-up of populations living at archaeolog- partially or completely replaced resident hunter-gatherers ically known times and places, ancient DNA makes it [3–6]. On the side of stasis, there are the ‘serial founder possible to directly track migrations and responses to effect’ models [7,8], which proposed that populations have natural selection. remained in the locations they first colonized after the out- of-Africa expansion, exchanging migrants only at a low Introduction rate with their immediate neighbors until the long-range Within the past 100 000 years anatomically modern migrations of the past 500 years [9–12]. humans have expanded to occupy every habitable area These genetic models – the wave-of-advance models on of the globe. The history of this expansion has been ex- the one hand, and the serial founder effect models on the plored with tools from several disciplines including linguis- other – were proposed before the availability of large-scale tics, archaeology, physical anthropology, and genetics. genomic data. The great synthesis of genetic data with These disciplines all can be used to ask the same question: historical, archaeological and linguistic information, ‘The how did we get to where we are today? History and Geography of Human Genes’ [13], was pub- Attempts to answer this question have often taken the lished in 1994 based on data from around 100 protein form of a dialectic between two hypotheses. On the one hand are arguments in favor of demographic stasis, which propose that the inhabitants of a region are the descen- Glossary dants of the first people to arrive there. On the other side Admixture: a sudden increase in gene flow between two differentiated are the arguments in favor of rapid demographic change, populations. Bottleneck: a temporary decrease in population size in the history of a Corresponding authors: Pickrell, J.K. ([email protected]); Reich, D. population. ([email protected]). Gene flow: the exchange of genes between two populations as a result of interbreeding. 0168-9525/ Heterozygosity: the number of differences between two random copies of a ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tig.2014.07.007 genome in a population. Trends in Genetics, September 2014, Vol. 30, No. 9 377 Feature Review Trends in Genetics September 2014, Vol. 30, No. 9 polymorphisms, and the papers that popularized the no- The observation of a smooth decline in human diversi- tion of a serial founder effect model were written based on ty with increasing geographic distance from Africa was data from around 1000 microsatellites. However, it is now interpreted as a window into demographic events deep in possible to genotype millions of polymorphisms in thou- our species’ past. Specifically, in the serial founder effect sands of individuals using high-throughput sequencing. and related models (Figure 1A) [12], the peopling of the Because of these technological advances, the past few years globe proceeded by an iterative process in which small have seen a dramatic increase in the quantity of data bands of individuals pushed into unoccupied territory, available for learning about human history. Equally im- experienced population expansions, and subsequently portant has been rapid innovation in methods for making gave rise to new small bands of individuals who then inferences from these data. We argue here that the tech- pushed further into unoccupied territory. This model has nological breakthroughs of the past few years motivate a two important features: a large number of expansions systematic reevaluation of human history using modern into new territory by small groups of individuals (and genomic tools – a new ‘History and Geography of Human concurrent bottlenecks), and little subsequent migration Genes’ that exploits many orders of magnitude more data [7–12]. As Prugnolle et al. [7] wrote: ‘what is clear...is that than the original synthesis. [this] pattern of constant loss of genetic diversity along In the first section of the paper we summarize what we colonisation routes could only have arisen through suc- see as major lessons from the recent literature. In particu- cessive bottlenecks of small amplitude as the range of our lar, it is now clear that the data contradict any model in species increased... The pattern we observe also suggests which the genetic structure of the world today is approxi- that subsequent migration was limited or at least very mately the same as it was immediately following the out- localised’. This qualitative conclusion was followed by of-Africa expansion. Instead, the past 50 000 years of more quantitative ones; in an explicit fit of the serial human history have witnessed major upheavals, such that founder effect model to data, Deshpande et al. [9] con- much of the geographic information about the first human cluded that ‘incorporation into existing models of ex- migrations has been overwritten by subsequent population change between neighbouring populations is essential, movements. However, the data also often contradict mod- but at a very low rate’. els of population replacement: when two distinct popula- This model has been influential in many fields. If it is tion groups come together during demographic expansions correct, then the difficult problem of identifying the geo- the result is often genetic admixture rather than complete graphic origin of all modern humans is reduced to the replacement. This suggests that new types of models – with simpler problem of finding the geographic region where admixture at their center – are necessary for describing people have the most genetic diversity [8]. This idea has key aspects of human history ([14–16] for early examples of been used extensively in discussions of human origins (e.g., admixture models). [27,28]). The model also provides a null hypothesis of In the second section of the paper we sketch out a way limited migration against which alternatives can be tested forward for data-driven construction of these models. We [29,30]. Outside genetics, the serial founder effect model specifically highlight the potential of ancient DNA studies has been used as a framework to interpret data from of individuals from archaeologically important cultures. linguistics [31], physical anthropology [32–35], material Such studies in principle provide a source of information culture [36], and economics [37]. about history that bypasses some fundamental ambigui- The serial founder effect model, however, is only one of ties in the interpretation of genetic, archaeological, or many models that can produce qualitatively similar pat- anthropological evidence alone. We discuss several poten- terns of genetic diversity (e.g., [38,39]). Producing the tial applications of this technology to outstanding ques- empirical pattern of a smooth decline in diversity with tions in human history. distance from Africa simply requires that the average time There are a number of excellent articles that have to the most recent common ancestor between two chromo- reviewed the literature on genome-wide