Resequencing Data Provide No Evidence for a Human Bottleneck in Africa during the Penultimate Glacial Period

Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.
Molecular Biology and Evolution (Impact Factor: 9.11). 02/2012; 29(7):1851-60. DOI: 10.1093/molbev/mss061
Source: PubMed


Based on the accumulation of genetic, climatic, and fossil evidence, a central theory in paleoanthropology stipulates that a demographic bottleneck coincided with the origin of our species Homo Sapiens. This theory proposes that anatomically modern humans--which were only present in Africa at the time--experienced a drastic bottleneck during the penultimate glacial age (130-190 kya) when a cold and dry climate prevailed. Two scenarios have been proposed to describe the bottleneck, which involve either a fragmentation of the range occupied by humans or the survival of one small group of humans. Here, we analyze DNA sequence data from 61 nuclear loci sequenced in three African populations using Approximate Bayesian Computation and numerical simulations. In contrast to the bottleneck theory, we show that a simple model without any bottleneck during the penultimate ice age has the greatest statistical support compared with bottleneck models. Although the proposed bottleneck is ancient, occurring at least 130 kya, we can discard the possibility that it did not leave detectable footprints in the DNA sequence data except if the bottleneck involves a less than a 3-fold reduction in population size. Finally, we confirm that a simple model without a bottleneck is able to reproduce the main features of the observed patterns of genetic variation. We conclude that models of Pleistocene refugium for modern human origins now require substantial revision.

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Available from: Michael GB Blum, May 22, 2014
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    • "Researchers have long been interested in using genetic data to infer population bottlenecks associated with landmark events in the history of species and populations, for example, the colonization of new regions or range contractions (reviewed in Gattepaille et al. 2013). Indeed, the demographic history of model organisms such as humans and Drosophila has been characterized as a series of expansions and contractions that coincide with the spread of populations across the globe (e.g., Haddrill et al. 2005; Voight et al. 2005; Sjödin et al. 2012). However, the genetic resources for model organisms far exceed those available for most species. "
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    ABSTRACT: The advent of the genomic era has necessitated the development of methods capable of analyzing large volumes of genomic data efficiently. Being able to reliably identify bottlenecks - extreme population size changes of short duration - is not only interesting in the context of speciation and extinction but also matters (as a null model) when inferring selection. Bottlenecks can be detected in polymorphism data via their distorting effect on the shape of the underlying genealogy. Here, we use the generating function of genealogies to derive the probability of mutational configurations in short sequence blocks under a simple bottleneck model. Given a large number of non-recombining blocks, we can compute maximum likelihood estimates of the time and strength of the bottleneck. Our method relies on a simple summary of the joint distribution of polymorphic sites. We extend the site frequency spectrum by counting mutations in frequency classes in short sequence blocks. Using linkage information over short distances in this way gives greater power to detect bottlenecks than the site frequency spectrum and potentially opens up a wide range of demographic histories to blockwise inference. Finally, we apply our method to genomic data from a species of pig (Sus cebifrons) endemic to islands in the center and west of the Philippines to estimate whether a bottleneck occurred upon island colonization and compare our scheme to Li and Durbin's pairwise sequentially Markovian coalescent (PSMC) both for the pig data and using simulations. Copyright © 2015, The Genetics Society of America.
    Genetics 09/2015; 201(3). DOI:10.1534/genetics.115.179861 · 5.96 Impact Factor
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    • "See Blum et al. (2013) for illustration in a parameter inference setting. Other work focuses on validating a particular choice of S. One approach is to run ABC analyses on a large number of simulated data sets to check whether S provides accurate results (Sjödin et al., 2012; Sousa et al., 2012). Marin et al. (2013) give a complementary approach, identifying necessary and sufficient properties of S for an ABC model choice analysis to be consistent in an asymptotic regime corresponding to highly informative data. "
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    ABSTRACT: Abstract A central statistical goal is to choose between alternative explanatory models of data. In many modern applications, such as population genetics, it is not possible to apply standard methods based on evaluating the likelihood functions of the models, as these are numerically intractable. Approximate Bayesian computation (ABC) is a commonly used alternative for such situations. ABC simulates data x for many parameter values under each model, which is compared to the observed data xobs. More weight is placed on models under which S(x) is close to S(xobs), where S maps data to a vector of summary statistics. Previous work has shown the choice of S is crucial to the efficiency and accuracy of ABC. This paper provides a method to select good summary statistics for model choice. It uses a preliminary step, simulating many x values from all models and fitting regressions to this with the model as response. The resulting model weight estimators are used as S in an ABC analysis. Theoretical results are given to justify this as approximating low dimensional sufficient statistics. A substantive application is presented: choosing between competing coalescent models of demographic growth for Campylobacter jejuni in New Zealand using multi-locus sequence typing data.
    Statistical Applications in Genetics and Molecular Biology 12/2013; 13(1):1-16. DOI:10.1515/sagmb-2013-0012 · 1.13 Impact Factor
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    • "No matter what species definition is used to describe the diversity of ancient humans—interbreeding human species or interbreeding populations of a single species—the issue of importance to us is whether or not there is a single recent unique ancestry for modern populations. There is wide agreement that there was no bottleneck at the origin of modern humans (Sjödin et al., 2012), and modern humans do not have a single unique ancestry in a recent African (or any other) population. "
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    ABSTRACT: The twenty-first century brought certainty to the understanding that people alive today and their immediate ancestors—modern humans—are not uniquely the descendants of a recent, small African population. Today's populations had multiple ancestors in the Middle Pleistocene and did not originate as a phylogenetic entity. The anatomical, behavioral, and genetic aspects of their modernity were not tied together in their origin. Instead, we propose a new understanding that anatomical modernity, behavioral modernity, and genetic modernity have different meanings that can be comprehended by viewing them as distinct interrelated processes. In this paper we discuss these processes and suggest that all three aspects of modernity are related in that they each characterize all living and recent human populations, and through a key unifying process: changes in human demographic history originating as the consequence of increased adult survivorship. The rapid increases in longevity in the Late Pleistocene took place in the context of other evolutionary changes and resulted in significant population size increases and increased numbers of population extinctions and replacements that affect genetic evolution. Perhaps the most important of these consequences is acceleration of natural selection with the appearance of more adaptive mutations, creating an evolutionary pattern that differs from archaic patterns in both tempo and mode. The modern pattern is one of increasingly rapid genetic, biological, and social changes within the widespread, interconnected human species. This way, modernity results in what we consider three of the most unique aspects of the recent and contemporary human species: its rapid, accelerating genetic evolution; the mixed ancestry of human populations and the absence of human races despite widespread geographic variation; and the social and adaptive consequences of multigenerational relationships, grandparents, and the wider kinship/social systems they support. We discuss how the processes of modernity became interrelated over time and all human populations became mixed as the demographic consequences of significant longevity developed.
    The Origins of Modern Humans, 07/2013: pages 355-391; , ISBN: 9780470894095
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