Inferring Population Histories for Ancient Genomes Using Genome-Wide Genealogies

Ancient genomes anchor genealogies in directly observed historical genetic variation and contextualize ancestral lineages with archaeological insights into their geography and cultural associations. However, the majority of ancient genomes are of lower coverage and cannot be directly built into genealogies. Here, we present a fast and scalable method, Colate, the first approach for inferring ancestral relationships through time between low-coverage genomes without requiring phasing or imputation. Our approach leverages sharing patterns of mutations dated using a genealogy to infer coalescence rates. For deeply sequenced ancient genomes, we additionally introduce an extension of the Relate algorithm for joint inference of genealogies incorporating such genomes. Application to 278 present-day and 430 ancient DNA samples of >0.5x mean coverage allows us to identify dynamic population structure and directional gene flow between early farmer and European hunter-gatherer groups. We further show that the previously reported, but still unexplained, increase in the TCC/TTC mutation rate, which is strongest in West Eurasia today, was already present at similar strength and widespread in the Late Glacial Period ~10k−15k years ago, but is not observed in samples >30k years old. It is strongest in Neolithic farmers, and highly correlated with recent coalescence rates between other genomes and a 10,000-year-old Anatolian hunter-gatherer. This suggests gene-flow among ancient peoples postdating the last glacial maximum as widespread and localizes the driver of this mutational signal in both time and geography in that region. Our approach should be widely applicable in future for addressing other evolutionary questions, and in other species.     

An ancient viral epidemic involving host coronavirus interacting genes more than 20,000 years ago in East Asia

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Ancient Human Genomes and Environmental DNA from the Cement Attaching 2,000-Year-Old Head Lice Nits

Over the past few decades, there has been a growing demand for genome analysis of ancient human remains. Destructive sampling is increasingly difficult to obtain for ethical reasons, and standard methods of breaking the skull to access the petrous bone or sampling remaining teeth are often forbidden for curatorial reasons. However, most ancient humans carried head lice and their eggs abound in historical hair specimens. Here we show that host DNA is protected by the cement that glues head lice nits to the hair of ancient Argentinian mummies, 1,500–2,000 years old. The genetic affinities deciphered from genome-wide analyses of this DNA inform that this population migrated from north-west Amazonia to the Andes of central-west Argentina; a result confirmed using the mitochondria of the host lice. The cement preserves ancient environmental DNA of the skin, including the earliest recorded case of Merkel cell polyomavirus. We found that the percentage of human DNA obtained from nit cement equals human DNA obtained from the tooth, yield 2-fold compared with a petrous bone, and 4-fold to a bloodmeal of adult lice a millennium younger. In metric studies of sheaths, the length of the cement negatively correlates with the age of the specimens, whereas hair linear distance between nit and scalp informs about the environmental conditions at the time before death. Ectoparasitic lice sheaths can offer an alternative, nondestructive source of high-quality ancient DNA from a variety of host taxa where bones and teeth are not available and reveal complementary details of their history.     

A consensus view of the proteome of the last universal common ancestor

The availability of genomic and proteomic data from across the tree of life has made it possible to infer features of the genome and proteome of the last universal common ancestor (LUCA). A number of studies have done so, all using a unique set of methods and bioinformatics databases. Here, we compare predictions across eight such studies and measure both their agreement with one another and with the consensus predictions among them. We find that some LUCA genome studies show a strong agreement with the consensus predictions of the others, but that no individual study shares a high or even moderate degree of similarity with any other individual study. From these observations, we conclude that the consensus among studies provides a more accurate depiction of the core proteome of the LUCA and its functional repertoire. The set of consensus LUCA protein family predictions between all of these studies portrays a LUCA genome that, at minimum, encoded functions related to protein synthesis, amino acid metabolism, nucleotide metabolism, and the use of common, nucleotide‐derived organic cofactors.     

THE TEMPO AND MODE OF EVOLUTION OF TRANSPOSABLE ELEMENTS AS REVEALED BY MOLECULAR PHYLOGENIES RECONSTRUCTED FROM MOSQUITO GENOMES

Although many mathematical models exist predicting the dynamics of transposable elements (TEs), there is a lack of available empirical data to validate these models and inherent assumptions. Genomes can provide a snapshot of several TE families in a single organism, and these could have their demographics inferred by coalescent analysis, allowing for the testing of theories on TE amplification dynamics. Using the available genomes of the mosquitoes Aedes aegypti and Anopheles gambiae, we indicate that such an approach is feasible. Our analysis follows four steps: (1) mining the two mosquito genomes currently available in search of TE families; (2) fitting, to selected families found in (1), a phylogeny tree under the general time‐reversible (GTR) nucleotide substitution model with an uncorrelated lognormal (UCLN) relaxed clock and a nonparametric demographic model; (3) fitting a nonparametric coalescent model to the tree generated in (2); and (4) fitting parametric models motivated by ecological theories to the curve generated in (3).     

Demic and cultural diffusion in prehistoric Europe in the age of ancient genomes

Ancient genomes can help us detect prehistoric migrations, population contractions, and admixture among populations. Knowing the dynamics of demography is invaluable for understanding culture change in prehistory, particularly the roles played by demic and cultural diffusion in transformations of material cultures. Prehistoric Europe is a region where ancient genome analyses can help illuminate the interplay between demography and culture change. In Europe, there is more archeological evidence, in terms of detailed studies, radiometric dates, and explanatory hypotheses that can be evaluated, than in any other region of the world. Here I show some important ways that ancient genomes have given us insights into population movements in European prehistory. I also propose that studies might be increasingly focused on specific questions of culture change, for example in evaluating the makers of “transitional” industries as well as the origins of the Gravettian and spread of the Magdalenian. I also discuss genomic evidence supporting the large role that demic expansion has played in the Neolithization of Europe and the formation of the European population during the Bronze Age.     

Archaeological mitogenomes illuminate the historical ecology of sea otters (Enhydra lutris) and the viability of reintroduction

Genetic analyses are an important contribution to wildlife reintroductions, particularly in the modern context of extirpations and ecological destruction. To address the complex historical ecology of the sea otter (Enhydra lutris) and its failed 1970s reintroduction to coastal Oregon, we compared mitochondrial genomes of pre-extirpation Oregon sea otters to extant and historical populations across the range. We sequenced, to our knowledge, the first complete ancient mitogenomes from archaeological Oregon sea otter dentine and historical sea otter dental calculus. Archaeological Oregon sea otters (n = 20) represent 10 haplotypes, which cluster with haplotypes from Alaska, Washington and British Columbia, and exhibit a clear division from California haplotypes. Our results suggest that extant northern populations are appropriate for future reintroduction efforts. This project demonstrates the feasibility of mitogenome capture and sequencing from non-human dental calculus and the diverse applications of ancient DNA analyses to pressing ecological and conservation topics and the management of at-risk/extirpated species.     

Microbial population genomes from the Amazon River reveal possible modulation of the organic matter degradation process in tropical freshwaters

Rivers connect the carbon cycle in land with that in aquatic ecosystems by transporting and transforming terrestrial organic matter (TeOM). The Amazon River receives huge loads of TeOM from the surrounding rainforest, promoting a substantial microbial heterotrophic activity and consequently, CO₂ outgassing. In the Amazon River, microbes degrade up to 55% of the lignin present in the TeOM. Yet, the main microbial genomes involved in TeOM degradation were unknown. Here, we characterize 51 population genomes (PGs) representing some of the most abundant microbes in the Amazon River deriving from 106 metagenomes. The 51 reconstructed PGs are among the most abundant microbes in the Amazon River, and 53% of them are not able to degrade TeOM. Among the PGs capable of degrading TeOM, 20% were exclusively cellulolytic, while the others could also oxidize lignin. The transport and consumption of lignin oxidation byproducts seemed to be decoupled from the oxidation process, being apparently performed by different groups of microorganisms. By connecting the genomic features of abundant microbes in the Amazon River with the degradation machinery of TeOM, we suggest that a complex microbial consortium could explain the quick turnover of TeOM previously observed in this ecosystem.     

Genetic Continuity of Bronze Age Ancestry with Increased Steppe-Related Ancestry in Late Iron Age Uzbekistan

Although Uzbekistan and Central Asia are known for the well-studied Bronze Age civilization of the Bactria–Margiana Archaeological Complex (BMAC), the lesser-known Iron Age was also a dynamic period that resulted in increased interaction and admixture among different cultures from this region. To broaden our understanding of events that impacted the demography and population structure of this region, we generated 27 genome-wide single-nucleotide polymorphism capture data sets of Late Iron Age individuals around the Historical Kushan time period (∼2100–1500 BP) from three sites in South Uzbekistan. Overall, Bronze Age ancestry persists into the Iron Age in Uzbekistan, with no major replacements of populations with Steppe-related ancestry. However, these individuals suggest diverse ancestries related to Iranian farmers, Anatolian farmers, and Steppe herders, with a small amount of West European Hunter Gatherer, East Asian, and South Asian Hunter Gatherer ancestry as well. Genetic affinity toward the Late Bronze Age Steppe herders and a higher Steppe-related ancestry than that found in BMAC populations suggest an increased mobility and interaction of individuals from the Northern Steppe in a Southward direction. In addition, a decrease of Iranian and an increase of Anatolian farmer-like ancestry in Uzbekistan Iron Age individuals were observed compared with the BMAC populations from Uzbekistan. Thus, despite continuity from the Bronze Age, increased admixture played a major role in the shift from the Bronze to the Iron Age in southern Uzbekistan. This mixed ancestry is also observed in other parts of the Steppe and Central Asia, suggesting more widespread admixture among local populations.     

Emerging genetic patterns of the European Neolithic: perspectives from a late Neolithic Bell Beaker burial site in Germany

The transition from hunting and gathering to agriculture in Europe is associated with demographic changes that may have shifted the human gene pool of the region as a result of an influx of Neolithic farmers from the Near East. However, the genetic composition of populations after the earliest Neolithic, when a diverse mosaic of societies that had been fully engaged in agriculture for some time appeared in central Europe, is poorly known. At this period during the Late Neolithic (ca. 2,800-2,000 BC), regionally distinctive burial patterns associated with two different cultural groups emerge, Bell Beaker and Corded Ware, and may reflect differences in how these societies were organized. Ancient DNA analyses of human remains from the Late Neolithic Bell Beaker site of Kromsdorf, Germany showed distinct mitochondrial haplotypes for six individuals, which were classified under the haplogroups I1, K1, T1, U2, U5, and W5, and two males were identified as belonging to the Y haplogroup R1b. In contrast to other Late Neolithic societies in Europe emphasizing maintenance of biological relatedness in mortuary contexts, the diversity of maternal haplotypes evident at Kromsdorf suggests that burial practices of Bell Beaker communities operated outside of social norms based on shared maternal lineages. Furthermore, our data, along with those from previous studies, indicate that modern U5-lineages may have received little, if any, contribution from the Mesolithic or Neolithic mitochondrial gene pool.     

Properties of 2-locus genealogies and linkage disequilibrium in temporally structured samples

Archeogenetics has been revolutionary, revealing insights into demographic history and recent positive selection. However, most studies to date have ignored the nonrandom association of genetic variants at different loci (i.e. linkage disequilibrium). This may be in part because basic properties of linkage disequilibrium in samples from different times are still not well understood. Here, we derive several results for summary statistics of haplotypic variation under a model with time-stratified sampling: (1) The correlation between the number of pairwise differences observed between time-staggered samples (πΔt) in models with and without strict population continuity; (2) The product of the linkage disequilibrium coefficient, D, between ancient and modern samples, which is a measure of haplotypic similarity between modern and ancient samples; and (3) The expected switch rate in the Li and Stephens haplotype copying model. The latter has implications for genotype imputation and phasing in ancient samples with modern reference panels. Overall, these results provide a characterization of how haplotype patterns are affected by sample age, recombination rates, and population sizes. We expect these results will help guide the interpretation and analysis of haplotype data from ancient and modern samples.     

Genomic Adaptations and Evolutionary History of the Extinct Scimitar-Toothed Cat,Homotherium latidens

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Mitochondrial genomes reveal the extinct Hippidion as an outgroup to all living equids

Hippidions were equids with very distinctive anatomical features. They lived in South America 2.5 million years ago (Ma) until their extinction approximately 10 000 years ago. The evolutionary origin of the three known Hippidion morphospecies is still disputed. Based on palaeontological data, Hippidion could have diverged from the lineage leading to modern equids before 10 Ma. In contrast, a much later divergence date, with Hippidion nesting within modern equids, was indicated by partial ancient mitochondrial DNA sequences. Here, we characterized eight Hippidion complete mitochondrial genomes at 3.4–386.3-fold coverage using target-enrichment capture and next-generation sequencing. Our dataset reveals that the two morphospecies sequenced (H. saldiasi and H. principale) formed a monophyletic clade, basal to extant and extinct Equus lineages. This contrasts with previous genetic analyses and supports Hippidion as a distinct genus, in agreement with palaeontological models. We date the Hippidion split from Equus at 5.6–6.5 Ma, suggesting an early divergence in North America prior to the colonization of South America, after the formation of the Panamanian Isthmus 3.5 Ma and the Great American Biotic Interchange.     

Spatio-temporal population genetics of the Danish pine marten (Martes martes)

A spatio-temporal study of genetic variation in the Danish pine marten ( Martes martes ) populations from the Jutland peninsula and from the island of Sealand was performed using 11 microsatellite markers. Samples obtained from 1892 to 2003 were subdivided into historical (prior to 1970) and recent (from 1970) groups. As compared with the historical samples, there was a significant loss of genetic variation in the recent Jutland population, but not in Sealand. Effective population sizes were estimated using Bayesian-based software (TMVP). Historical effective population sizes were 5897 (90% highest probability density, HPD, limits: 1502–6849) in Jutland and 1300 (90% HPD limits: 224–5929) in Sealand, whereas recent effective population sizes were 14.7 (90% HPD limits: 10.9–23.5) in Jutland and 802 (90% HPD limits: 51.8–5510) in Sealand. Significant genetic differentiation ( F _ST) was found between the two historical samples, between the two recent samples, and between the historical and the recent sample in Jutland; whereas the F _ST value between the historical and the recent sample in Sealand was not significant. The significant genetic differentiation between the historical and the recent samples indicates changes in the genetic compositions over time, and the higher F _ST values between the two recent samples, as compared with the two historical samples, indicates that the populations in Sealand and Jutland have drifted apart within a short time span. No deviation from Hardy–Weinberg equilibrium was found within populations, indicating no further substructuring.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 457–464.     

Pleistocene mitogenomes reconstructed from the environmental DNA of permafrost sediments

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