Human evolution: a tale from ancient genomes Llamas, Bastien; Willerslev, Eske; Orlando, Ludovic
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
02/2017, Volume:
372, Issue:
1713
Journal Article
Peer reviewed
Open access
The field of human ancient DNA (aDNA) has moved from mitochondrial sequencing that suffered from contamination and provided limited biological insights, to become a fully genomic discipline that is ...changing our conception of human history. Recent successes include the sequencing of extinct hominins, and true population genomic studies of Bronze Age populations. Among the emerging areas of aDNA research, the analysis of past epigenomes is set to provide more new insights into human adaptation and disease susceptibility through time. Starting as a mere curiosity, ancient human genetics has become a major player in the understanding of our evolutionary history.
This article is part of the themed issue ‘Evo-devo in the genomics era, and the origins of morphological diversity’.
Genetic time‐series data from historical samples greatly facilitate inference of past population dynamics and species evolution. Yet, although climate and landscape change are often touted as ...post‐hoc explanations of biological change, our understanding of past climate and landscape change influences on evolutionary processes is severely hindered by the limited application of methods that directly relate environmental change to species dynamics through time. Increased integration of spatiotemporal environmental and genetic data will revolutionize the interpretation of environmental influences on past population processes and the quantification of recent anthropogenic impacts on species, and vastly improve prediction of species responses under future climate change scenarios, yielding widespread revelations across evolutionary biology, landscape ecology and conservation genetics. This review encourages greater use of spatiotemporal landscape genetic analyses that explicitly link landscape, climate and genetic data through time by providing an overview of analytical approaches for integrating historical genetic and environmental data in five key research areas: population genetic structure, demography, phylogeography, metapopulation connectivity and adaptation. We also include a tabular summary of key methodological information, suggest approaches for mitigating the particular difficulties in applying these techniques to ancient DNA and palaeoclimate data, and highlight areas for future methodological development.
We generated genome-wide data from 69 Europeans who lived between 8,000-3,000 years ago by enriching ancient DNA libraries for a target set of almost 400,000 polymorphisms. Enrichment of these ...positions decreases the sequencing required for genome-wide ancient DNA analysis by a median of around 250-fold, allowing us to study an order of magnitude more individuals than previous studies and to obtain new insights about the past. We show that the populations of Western and Far Eastern Europe followed opposite trajectories between 8,000-5,000 years ago. At the beginning of the Neolithic period in Europe, ∼8,000-7,000 years ago, closely related groups of early farmers appeared in Germany, Hungary and Spain, different from indigenous hunter-gatherers, whereas Russia was inhabited by a distinctive population of hunter-gatherers with high affinity to a ∼24,000-year-old Siberian. By ∼6,000-5,000 years ago, farmers throughout much of Europe had more hunter-gatherer ancestry than their predecessors, but in Russia, the Yamnaya steppe herders of this time were descended not only from the preceding eastern European hunter-gatherers, but also from a population of Near Eastern ancestry. Western and Eastern Europe came into contact ∼4,500 years ago, as the Late Neolithic Corded Ware people from Germany traced ∼75% of their ancestry to the Yamnaya, documenting a massive migration into the heartland of Europe from its eastern periphery. This steppe ancestry persisted in all sampled central Europeans until at least ∼3,000 years ago, and is ubiquitous in present-day Europeans. These results provide support for a steppe origin of at least some of the Indo-European languages of Europe.
The peopling of Sahul (the combined continent of Australia and New Guinea) represents the earliest continental migration and settlement event of solely anatomically modern humans, but its patterns ...and ecological drivers remain largely conceptual in the current literature. We present an advanced stochastic-ecological model to test the relative support for scenarios describing where and when the first humans entered Sahul, and their most probable routes of early settlement. The model supports a dominant entry via the northwest Sahul Shelf first, potentially followed by a second entry through New Guinea, with initial entry most consistent with 50,000 or 75,000 years ago based on comparison with bias-corrected archaeological map layers. The model's emergent properties predict that peopling of the entire continent occurred rapidly across all ecological environments within 156-208 human generations (4368-5599 years) and at a plausible rate of 0.71-0.92 km year
. More broadly, our methods and approaches can readily inform other global migration debates, with results supporting an exit of anatomically modern humans from Africa 63,000-90,000 years ago, and the peopling of Eurasia in as little as 12,000-15,000 years via inland routes.
We report detailed peptide‐binding affinities between 438 HLA Class I and Class II proteins and complete proteomes of seven pandemic human viruses, including coronaviruses, influenza viruses and ...HIV‐1. We contrast these affinities with HLA allele frequencies across hundreds of human populations worldwide. Statistical modelling shows that peptide‐binding affinities classified into four distinct categories depend on the HLA locus but that the type of virus is only a weak predictor, except in the case of HIV‐1. Among the strong HLA binders (IC50 ≤ 50), we uncovered 16 alleles (the top ones being A*02:02, B*15:03 and DRB1*01:02) binding more than 1% of peptides derived from all viruses, 9 (top ones including HLA‐A*68:01, B*15:25, C*03:02 and DRB1*07:01) binding all viruses except HIV‐1, and 15 (top ones A*02:01 and C*14:02) only binding coronaviruses. The frequencies of strongest and weakest HLA peptide binders differ significantly among populations from different geographic regions. In particular, Indigenous peoples of America show both higher frequencies of strongest and lower frequencies of weakest HLA binders. As many HLA proteins are found to be strong binders of peptides derived from distinct viral families, and are hence promiscuous (or generalist), we discuss this result in relation to possible signatures of natural selection on HLA promiscuous alleles due to past pathogenic infections. Our findings are highly relevant for both evolutionary genetics and the development of vaccine therapies. However they should not lead to forget that individual resistance and vulnerability to diseases go beyond the sole HLA allelic affinity and depend on multiple, complex and often unknown biological, environmental and other variables.
The evolution of the ratite birds has been widely attributed to vicariant speciation, driven by the Cretaceous breakup of the supercontinent Gondwana. The early isolation of Africa and Madagascar ...implies that the ostrich and extinct Madagascan elephant birds (Aepyornithidae) should be the oldest ratite lineages. We sequenced the mitochondrial genomes of two elephant birds and performed phylogenetic analyses, which revealed that these birds are the closest relatives of the New Zealand kiwi and are distant from the basal ratite lineage of ostriches. This unexpected result strongly contradicts continental vicariance and instead supports flighted dispersal in all major ratite lineages. We suggest that convergence toward gigantism and flightlessness was facilitated by early Tertiary expansion into the diurnal herbivory niche after the extinction of the dinosaurs.
British population history has been shaped by a series of immigrations, including the early Anglo-Saxon migrations after 400 CE. It remains an open question how these events affected the genetic ...composition of the current British population. Here, we present whole-genome sequences from 10 individuals excavated close to Cambridge in the East of England, ranging from the late Iron Age to the middle Anglo-Saxon period. By analysing shared rare variants with hundreds of modern samples from Britain and Europe, we estimate that on average the contemporary East English population derives 38% of its ancestry from Anglo-Saxon migrations. We gain further insight with a new method, rarecoal, which infers population history and identifies fine-scale genetic ancestry from rare variants. Using rarecoal we find that the Anglo-Saxon samples are closely related to modern Dutch and Danish populations, while the Iron Age samples share ancestors with multiple Northern European populations including Britain.
Xu et al. (2021) recently recommended a new parameterization of BWA‐mem as a superior alternative to the widely‐used BWA‐aln algorithm to map ancient DNA sequencing data. Here, we compare the BWA‐mem ...parameterization recommended by Xu et al. with the best‐performing alignment methods determined in the recent benchmarks of Oliva and colleagues (2021), demonstrating that BWA‐aln is still the gold‐standard for ancient DNA read alignment .
The ability of our ancestors to switch food sources and to migrate to more favourable environments enabled the rapid global expansion of anatomically modern humans beyond Africa as early as 120,000 ...years ago. Whether this versatility was largely the result of environmentally determined processes or was instead dominated by cultural drivers, social structures, and interactions among different groups, is unclear. We develop a statistical approach that combines both archaeological and genetic data to infer the more-likely initial expansion routes in northern Eurasia and the Americas. We then quantify the main differences in past environmental conditions between the more-likely routes and other potential (less-likely) routes of expansion. We establish that, even though cultural drivers remain plausible at finer scales, the emergent migration corridors were predominantly constrained by a combination of regional environmental conditions, including the presence of a forest-grassland ecotone, changes in temperature and precipitation, and proximity to rivers.
High-Throughput DNA Sequencing (HTS) technologies have changed the way in which we detect and assess DNA contamination in ancient DNA studies. Researchers use computational methods to mine the large ...quantity of sequencing data to detect characteristic patterns of DNA damage, and to evaluate the authenticity of the results. We argue that unless computational methods can confidently separate authentic ancient DNA sequences from contaminating DNA that displays damage patterns under independent decay processes, prevention and control of DNA contamination should remain a central and critical aspect of ancient human DNA studies. Ideally, DNA contamination can be prevented early on by following minimal guidelines during excavation, sample collection and/or subsequent handling. Contaminating DNA should also be monitored or minimised in the ancient DNA laboratory using specialised facilities and strict experimental procedures. In this paper, we update recommendations to control for DNA contamination from the field to the laboratory, in an attempt to facilitate communication between field archaeologists, anthropologists and ancient DNA researchers. We also provide updated criteria of ancient DNA authenticity for HTS-based studies. We are confident that the procedures outlined here will increase the retrieval of higher proportions of authentic genetic information from valuable archaeological human remains in the future.
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