Publications by authors named "Ludovic Orlando"

172 Publications

The origins and spread of domestic horses from the Western Eurasian steppes.

Nature 2021 Oct 20;598(7882):634-640. Epub 2021 Oct 20.

UMR 5199 De la Préhistoire à l'Actuel : Culture, Environnement et Anthropologie (PACEA), CNRS, Université de Bordeaux, Pessac Cedex, France.

Domestication of horses fundamentally transformed long-range mobility and warfare. However, modern domesticated breeds do not descend from the earliest domestic horse lineage associated with archaeological evidence of bridling, milking and corralling at Botai, Central Asia around 3500 BC. Other longstanding candidate regions for horse domestication, such as Iberia and Anatolia, have also recently been challenged. Thus, the genetic, geographic and temporal origins of modern domestic horses have remained unknown. Here we pinpoint the Western Eurasian steppes, especially the lower Volga-Don region, as the homeland of modern domestic horses. Furthermore, we map the population changes accompanying domestication from 273 ancient horse genomes. This reveals that modern domestic horses ultimately replaced almost all other local populations as they expanded rapidly across Eurasia from about 2000 BC, synchronously with equestrian material culture, including Sintashta spoke-wheeled chariots. We find that equestrianism involved strong selection for critical locomotor and behavioural adaptations at the GSDMC and ZFPM1 genes. Our results reject the commonly held association between horseback riding and the massive expansion of Yamnaya steppe pastoralists into Europe around 3000 BC driving the spread of Indo-European languages. This contrasts with the scenario in Asia where Indo-Iranian languages, chariots and horses spread together, following the early second millennium BC Sintashta culture.
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http://dx.doi.org/10.1038/s41586-021-04018-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8550961PMC
October 2021

Late Quaternary dynamics of Arctic biota from ancient environmental genomics.

Nature 2021 Dec 20;600(7887):86-92. Epub 2021 Oct 20.

Center for Environmental Management of Military Lands, Colorado State University, Fort Collins, CO, USA.

During the last glacial-interglacial cycle, Arctic biotas experienced substantial climatic changes, yet the nature, extent and rate of their responses are not fully understood. Here we report a large-scale environmental DNA metagenomic study of ancient plant and mammal communities, analysing 535 permafrost and lake sediment samples from across the Arctic spanning the past 50,000 years. Furthermore, we present 1,541 contemporary plant genome assemblies that were generated as reference sequences. Our study provides several insights into the long-term dynamics of the Arctic biota at the circumpolar and regional scales. Our key findings include: (1) a relatively homogeneous steppe-tundra flora dominated the Arctic during the Last Glacial Maximum, followed by regional divergence of vegetation during the Holocene epoch; (2) certain grazing animals consistently co-occurred in space and time; (3) humans appear to have been a minor factor in driving animal distributions; (4) higher effective precipitation, as well as an increase in the proportion of wetland plants, show negative effects on animal diversity; (5) the persistence of the steppe-tundra vegetation in northern Siberia enabled the late survival of several now-extinct megafauna species, including the woolly mammoth until 3.9 ± 0.2 thousand years ago (ka) and the woolly rhinoceros until 9.8 ± 0.2 ka; and (6) phylogenetic analysis of mammoth environmental DNA reveals a previously unsampled mitochondrial lineage. Our findings highlight the power of ancient environmental metagenomics analyses to advance understanding of population histories and long-term ecological dynamics.
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http://dx.doi.org/10.1038/s41586-021-04016-xDOI Listing
December 2021

Performance and automation of ancient DNA capture with RNA hyRAD probes.

Mol Ecol Resour 2021 Sep 28. Epub 2021 Sep 28.

Centre d'Anthropobiologie et de Génomique de Toulouse (CAGT), Université Paul Sabatier, Faculté de Médecine Purpan, Toulouse, France.

DNA hybridization-capture techniques allow researchers to focus their sequencing efforts on preselected genomic regions. This feature is especially useful when analysing ancient DNA (aDNA) extracts, which are often dominated by exogenous environmental sources. Here, we assessed, for the first time, the performance of hyRAD as an inexpensive and design-free alternative to commercial capture protocols to obtain authentic aDNA data from osseous remains. HyRAD relies on double enzymatic restriction of fresh DNA extracts to produce RNA probes that cover only a fraction of the genome and can serve as baits for capturing homologous fragments from aDNA libraries. We found that this approach could retrieve sequence data from horse remains coming from a range of preservation environments, including beyond radiocarbon range, yielding up to 146.5-fold on-target enrichment for aDNA extracts showing extremely low endogenous content (<1%). Performance was, however, more limited for those samples already characterized by good DNA preservation (>20%-30%), while the fraction of endogenous reads mapping on- and off-target was relatively insensitive to the original endogenous DNA content. Procedures based on two instead of a single round of capture increased on-target coverage up to 3.6-fold. Additionally, we used methylation-sensitive restriction enzymes to produce probes targeting hypomethylated regions, which improved data quality by reducing post-mortem DNA damage and mapping within multicopy regions. Finally, we developed a fully automated hyRAD protocol utilizing inexpensive robotic platforms to facilitate capture processing. Overall, our work establishes hyRAD as a cost-effective strategy to recover a set of shared orthologous variants across multiple ancient samples.
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http://dx.doi.org/10.1111/1755-0998.13518DOI Listing
September 2021

No particular genomic features underpin the dramatic economic consequences of 17 century plague epidemics in Italy.

iScience 2021 Apr 31;24(4):102383. Epub 2021 Mar 31.

Centre for Anthropobiology and Genomics of Toulouse CAGT, UMR 5288, CNRS, Université Toulouse III Paul Sabatier, Faculté de Médecine Purpan, Bâtiment A, 37 allées Jules Guesde, 31000 Toulouse, France.

The 17 century plague epidemic had a particularly strong demographic toll in Southern Europe, especially Italy, where it caused long-lasting economical damage. Whether this resulted from ineffective sanitation measures or more pathogenic strains remains unknown. DNA screening of 26 skeletons from the 1629-1630 plague cemetery of Lariey (French Alps) identified two teeth rich in plague genetic material. Further sequencing revealed two genomes phylogenetically closest to those from the 1636 outbreak of San Procolo a Naturno, Italy. They both belonged to a cluster extending from the Alps to Northern Germany that probably propagated during the Thirty Years war. Sequence variation did not support faster evolutionary rates in the Italian genomes and revealed only rare private non-synonymous mutations not affecting virulence genes. This, and the more heterogeneous spatial diffusion of the epidemic outside Italy, suggests environmental or social rather than biological causes for the severe Italian epidemic trajectory.
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http://dx.doi.org/10.1016/j.isci.2021.102383DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8082092PMC
April 2021

Ancient horse genomes reveal the timing and extent of dispersals across the Bering Land Bridge.

Mol Ecol 2021 Dec 27;30(23):6144-6161. Epub 2021 May 27.

Biomolecular Engineering, University of California Santa Cruz, Santa Cruz, CA, USA.

The Bering Land Bridge (BLB) last connected Eurasia and North America during the Late Pleistocene. Although the BLB would have enabled transfers of terrestrial biota in both directions, it also acted as an ecological filter whose permeability varied considerably over time. Here we explore the possible impacts of this ecological corridor on genetic diversity within, and connectivity among, populations of a once wide-ranging group, the caballine horses (Equus spp.). Using a panel of 187 mitochondrial and eight nuclear genomes recovered from present-day and extinct caballine horses sampled across the Holarctic, we found that Eurasian horse populations initially diverged from those in North America, their ancestral continent, around 1.0-0.8 million years ago. Subsequent to this split our mitochondrial DNA analysis identified two bidirectional long-range dispersals across the BLB ~875-625 and ~200-50 thousand years ago, during the Middle and Late Pleistocene. Whole genome analysis indicated low levels of gene flow between North American and Eurasian horse populations, which probably occurred as a result of these inferred dispersals. Nonetheless, mitochondrial and nuclear diversity of caballine horse populations retained strong phylogeographical structuring. Our results suggest that barriers to gene flow, currently unidentified but possibly related to habitat distribution across Beringia or ongoing evolutionary divergence, played an important role in shaping the early genetic history of caballine horses, including the ancestors of living horses within Equus ferus.
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http://dx.doi.org/10.1111/mec.15977DOI Listing
December 2021

Evidence for early dispersal of domestic sheep into Central Asia.

Nat Hum Behav 2021 09 8;5(9):1169-1179. Epub 2021 Apr 8.

ArchaeoZOOlogy in Siberia and Central Asia - ZooSCAn, CNRS - IAET SB RAS International Research Laboratory, IRL 2013, Institute of Archaeology SB RAS, Novosibirsk, Russia.

The development and dispersal of agropastoralism transformed the cultural and ecological landscapes of the Old World, but little is known about when or how this process first impacted Central Asia. Here, we present archaeological and biomolecular evidence from Obishir V in southern Kyrgyzstan, establishing the presence of domesticated sheep by ca. 6,000 BCE. Zooarchaeological and collagen peptide mass fingerprinting show exploitation of Ovis and Capra, while cementum analysis of intact teeth implicates possible pastoral slaughter during the fall season. Most significantly, ancient DNA reveals these directly dated specimens as the domestic O. aries, within the genetic diversity of domesticated sheep lineages. Together, these results provide the earliest evidence for the use of livestock in the mountains of the Ferghana Valley, predating previous evidence by 3,000 years and suggesting that domestic animal economies reached the mountains of interior Central Asia far earlier than previously recognized.
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http://dx.doi.org/10.1038/s41562-021-01083-yDOI Listing
September 2021

Heterogeneous Hunter-Gatherer and Steppe-Related Ancestries in Late Neolithic and Bell Beaker Genomes from Present-Day France.

Curr Biol 2021 03;31(5):1072-1083.e10

Centre d'Anthropobiologie et de Génomique de Toulouse CAGT, CNRS UMR 5288, Université Toulouse III Paul Sabatier, Faculté de Médecine Purpan, Bâtiment A, 37 allées Jules Guesde, 31000 Toulouse, France. Electronic address:

The transition from the Late Neolithic to the Bronze Age has witnessed important population and societal changes in western Europe. These include massive genomic contributions of pastoralist herders originating from the Pontic-Caspian steppes into local populations, resulting from complex interactions between collapsing hunter-gatherers and expanding farmers of Anatolian ancestry. This transition is documented through extensive ancient genomic data from present-day Britain, Ireland, Iberia, Mediterranean islands, and Germany. It remains, however, largely overlooked in France, where most focus has been on the Middle Neolithic (n = 63), with the exception of one Late Neolithic genome sequenced at 0.05× coverage. This leaves the key transitional period covering ∼3,400-2,700 cal. years (calibrated years) BCE genetically unsampled and thus the exact time frame of hunter-gatherer persistence and arrival of steppe migrations unknown. To remediate this, we sequenced 24 ancient human genomes from France spanning ∼3,400-1,600 cal. years BCE. This reveals Late Neolithic populations that are genetically diverse and include individuals with dark skin, hair, and eyes. We detect heterogeneous hunter-gatherer ancestries within Late Neolithic communities, reaching up to ∼63.3% in some individuals, and variable genetic contributions of steppe herders in Bell Beaker populations. We provide an estimate as late as ∼3,800 years BCE for the admixture between Neolithic and Mesolithic populations and as early as ∼2,650 years BCE for the arrival of steppe-related ancestry. The genomic heterogeneity characterized underlines the complex history of human interactions even at the local scale.
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http://dx.doi.org/10.1016/j.cub.2020.12.015DOI Listing
March 2021

Genomics and the Evolutionary History of Equids.

Annu Rev Anim Biosci 2021 02 16;9:81-101. Epub 2020 Nov 16.

Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse, CNRS UMR 5288, Université Paul Sabatier, Toulouse 31000, France; email:

The equid family contains only one single extant genus, , including seven living species grouped into horses on the one hand and zebras and asses on the other. In contrast, the equine fossil record shows that an extraordinarily richer diversity existed in the past and provides multiple examples of a highly dynamic evolution punctuated by several waves of explosive radiations and extinctions, cross-continental migrations, and local adaptations. In recent years, genomic technologies have provided new analytical solutions that have enhanced our understanding of equine evolution, including the species radiation within ; the extinction dynamics of several lineages; and the domestication history of two individual species, the horse and the donkey. Here, we provide an overview of these recent developments and suggest areas for further research.
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http://dx.doi.org/10.1146/annurev-animal-061220-023118DOI Listing
February 2021

Genetic diversity, evolution and selection in the major histocompatibility complex DRB and DQB loci in the family Equidae.

BMC Genomics 2020 Sep 30;21(1):677. Epub 2020 Sep 30.

Department of Animal Genetics, Veterinary and Pharmaceutical University, Brno, Czech Republic.

Background: The mammalian Major Histocompatibility Complex (MHC) is a genetic region containing highly polymorphic genes with immunological functions. MHC class I and class II genes encode antigen-presenting molecules expressed on the cell surface. The MHC class II sub-region contains genes expressed in antigen presenting cells. The antigen binding site is encoded by the second exon of genes encoding antigen presenting molecules. The exon 2 sequences of these MHC genes have evolved under the selective pressure of pathogens. Interspecific differences can be observed in the class II sub-region. The family Equidae includes a variety of domesticated, and free-ranging species inhabiting a range of habitats exposed to different pathogens and represents a model for studying this important part of the immunogenome. While equine MHC class II DRA and DQA loci have received attention, the genetic diversity and effects of selection on DRB and DQB loci have been largely overlooked. This study aimed to provide the first in-depth analysis of the MHC class II DRB and DQB loci in the Equidae family.

Results: Three DRB and two DQB genes were identified in the genomes of all equids. The genes DRB2, DRB3 and DQB3 showed high sequence conservation, while polymorphisms were more frequent at DRB1 and DQB1 across all species analyzed. DQB2 was not found in the genome of the Asiatic asses Equus hemionus kulan and E. h. onager. The bioinformatic analysis of non-zero-coverage-bases of DRB and DQB genes in 14 equine individual genomes revealed differences among individual genes. Evidence for recombination was found for DRB1, DRB2, DQB1 and DQB2 genes. Trans-species allele sharing was identified in all genes except DRB1. Site-specific selection analysis predicted genes evolving under positive selection both at DRB and DQB loci. No selected amino acid sites were identified in DQB3.

Conclusions: The organization of the MHC class II sub-region of equids is similar across all species of the family. Genomic sequences, along with phylogenetic trees suggesting effects of selection as well as trans-species polymorphism support the contention that pathogen-driven positive selection has shaped the MHC class II DRB/DQB sub-regions in the Equidae.
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http://dx.doi.org/10.1186/s12864-020-07089-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7525986PMC
September 2020

The Evolutionary and Historical Foundation of the Modern Horse: Lessons from Ancient Genomics.

Authors:
Ludovic Orlando

Annu Rev Genet 2020 11 22;54:563-581. Epub 2020 Sep 22.

Laboratoire d'Anthropobiologie Moléculaire et Imagerie de Synthèse, Faculté de Médecine Purpan, Université Toulouse III-Paul Sabatier, 31000 Toulouse, France; email:

The domestication of the horse some 5,500 years ago followed those of dogs, sheep, goats, cattle, and pigs by ∼2,500-10,000 years. By providing fast transportation and transforming warfare, the horse had an impact on human history with no equivalent in the animal kingdom. Even though the equine sport industry has considerable economic value today, the evolutionary history underlying the emergence of the modern domestic horse remains contentious. In the last decade, novel sequencing technologies have revolutionized our capacity to sequence the complete genome of organisms, including from archaeological remains. Applied to horses, these technologies have provided unprecedented levels of information and have considerably changed models of horse domestication. This review illustrates how ancient DNA, especially ancient genomes, has inspired researchers to rethink the process by which horses were first domesticated and then diversified into a variety of breeds showing a range of traits that are useful to humans.
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http://dx.doi.org/10.1146/annurev-genet-021920-011805DOI Listing
November 2020

Population genomics of the Viking world.

Nature 2020 09 16;585(7825):390-396. Epub 2020 Sep 16.

NTNU University Museum, Department of Archaeology and Cultural History, Trondheim, Norway.

The maritime expansion of Scandinavian populations during the Viking Age (about AD 750-1050) was a far-flung transformation in world history. Here we sequenced the genomes of 442 humans from archaeological sites across Europe and Greenland (to a median depth of about 1×) to understand the global influence of this expansion. We find the Viking period involved gene flow into Scandinavia from the south and east. We observe genetic structure within Scandinavia, with diversity hotspots in the south and restricted gene flow within Scandinavia. We find evidence for a major influx of Danish ancestry into England; a Swedish influx into the Baltic; and Norwegian influx into Ireland, Iceland and Greenland. Additionally, we see substantial ancestry from elsewhere in Europe entering Scandinavia during the Viking Age. Our ancient DNA analysis also revealed that a Viking expedition included close family members. By comparing with modern populations, we find that pigmentation-associated loci have undergone strong population differentiation during the past millennium, and trace positively selected loci-including the lactase-persistence allele of LCT and alleles of ANKA that are associated with the immune response-in detail. We conclude that the Viking diaspora was characterized by substantial transregional engagement: distinct populations influenced the genomic makeup of different regions of Europe, and Scandinavia experienced increased contact with the rest of the continent.
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http://dx.doi.org/10.1038/s41586-020-2688-8DOI Listing
September 2020

Using paleo-archives to safeguard biodiversity under climate change.

Science 2020 08;369(6507)

Center for Macroecology, Evolution, and Climate, GLOBE Institute, University of Copenhagen, Copenhagen Ø 2100, Denmark.

Strategies for 21st-century environmental management and conservation under global change require a strong understanding of the biological mechanisms that mediate responses to climate- and human-driven change to successfully mitigate range contractions, extinctions, and the degradation of ecosystem services. Biodiversity responses to past rapid warming events can be followed in situ and over extended periods, using cross-disciplinary approaches that provide cost-effective and scalable information for species' conservation and the maintenance of resilient ecosystems in many bioregions. Beyond the intrinsic knowledge gain such integrative research will increasingly provide the context, tools, and relevant case studies to assist in mitigating climate-driven biodiversity losses in the 21st century and beyond.
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http://dx.doi.org/10.1126/science.abc5654DOI Listing
August 2020

Filling Important Gaps in the Genomic History of Southwest Asia.

Authors:
Ludovic Orlando

Cell 2020 05;181(5):966-968

Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse, CNRS UMR 5288, Université de Toulouse, Université Paul Sabatier, 31000 Toulouse, France; Globe Institute, Lundbeck Foundation GeoGenetics Centre, University of Copenhagen, 1350K Copenhagen, Denmark. Electronic address:

Many crucial developments in human prehistory occurred in Southwest Asia, including the transition to agriculture as well as the emergence of writing and of the earliest civilization. Two new studies in this issue of Cell map the genetic composition of human groups inhabiting the region during the sixth and first millennia Before Common Era (BCE) and uncover periods of significant population turnover.
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http://dx.doi.org/10.1016/j.cell.2020.05.010DOI Listing
May 2020

Museomics identifies genetic erosion in two butterfly species across the 20th century in Finland.

Mol Ecol Resour 2020 Sep 14;20(5):1191-1205. Epub 2020 May 14.

Geneva Natural History Museum, Geneva, Switzerland.

Erosion of biodiversity generated by anthropogenic activities has been studied for decades and in many areas at the species level, using taxa monitoring. In contrast, genetic erosion within species has rarely been tracked, and is often studied by inferring past population dynamics from contemporaneous estimators. An alternative to such inferences is the direct examination of past genes, by analysing museum collection specimens. While providing direct access to genetic variation over time, historical DNA is usually not optimally preserved, and it is necessary to apply genotyping methods based on hybridization-capture to unravel past genetic variation. In this study, we apply such a method (i.e., HyRAD), to large time series of two butterfly species in Finland, and present a new bioinformatic pipeline, namely PopHyRAD, that standardizes and optimizes the analysis of HyRAD data at the within-species level. In the localities for which the data retrieved have sufficient power to accurately examine genetic dynamics through time, we show that genetic erosion has increased across the last 100 years, as revealed by signatures of allele extinctions and heterozygosity decreases, despite local variations. In one of the two butterflies (Erebia embla), isolation by distance also increased through time, revealing the effect of greater habitat fragmentation over time.
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http://dx.doi.org/10.1111/1755-0998.13167DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7540272PMC
September 2020

Author Correction: Spotted phenotypes in horses lost attractiveness in the Middle Ages.

Sci Rep 2020 Apr 10;10(1):6469. Epub 2020 Apr 10.

Department of Evolutionary Genetics, Leibniz Institute for Zoo and Wildlife Research, 10315, Berlin, Germany.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41598-020-62905-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7148289PMC
April 2020

Animal domestication in the era of ancient genomics.

Nat Rev Genet 2020 08 7;21(8):449-460. Epub 2020 Apr 7.

Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse, CNRS UMR 5288, Université de Toulouse, Université Paul Sabatier, Toulouse, France.

The domestication of animals led to a major shift in human subsistence patterns, from a hunter-gatherer to a sedentary agricultural lifestyle, which ultimately resulted in the development of complex societies. Over the past 15,000 years, the phenotype and genotype of multiple animal species, such as dogs, pigs, sheep, goats, cattle and horses, have been substantially altered during their adaptation to the human niche. Recent methodological innovations, such as improved ancient DNA extraction methods and next-generation sequencing, have enabled the sequencing of whole ancient genomes. These genomes have helped reconstruct the process by which animals entered into domestic relationships with humans and were subjected to novel selection pressures. Here, we discuss and update key concepts in animal domestication in light of recent contributions from ancient genomics.
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http://dx.doi.org/10.1038/s41576-020-0225-0DOI Listing
August 2020

Dairy pastoralism sustained eastern Eurasian steppe populations for 5,000 years.

Nat Ecol Evol 2020 03 2;4(3):346-355. Epub 2020 Mar 2.

Department of Archaeology, Max Planck Institute for the Science of Human History, Jena, Germany.

Dairy pastoralism is integral to contemporary and past lifeways on the eastern Eurasian steppe, facilitating survival in agriculturally challenging environments. While previous research has indicated that ruminant dairy pastoralism was practiced in the region by circa 1300 BC, the origin, extent and diversity of this custom remain poorly understood. Here, we analyse ancient proteins from human dental calculus recovered from geographically diverse locations across Mongolia and spanning 5,000 years. We present the earliest evidence for dairy consumption on the eastern Eurasian steppe by circa 3000 BC and the later emergence of horse milking at circa 1200 BC, concurrent with the first evidence for horse riding. We argue that ruminant dairying contributed to the demographic success of Bronze Age Mongolian populations and that the origins of traditional horse dairy products in eastern Eurasia are closely tied to the regional emergence of mounted herding societies during the late second millennium BC.
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http://dx.doi.org/10.1038/s41559-020-1120-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7212056PMC
March 2020

Ancient Genomes Reveal Unexpected Horse Domestication and Management Dynamics.

Authors:
Ludovic Orlando

Bioessays 2020 01 6;42(1):e1900164. Epub 2019 Dec 6.

Laboratoire d'Anthropobiologie et d'Imagerie de Synthèse, CNRS UMR 5288, Faculté de Médecine de Purpan, 37 allées Jules Guesde, Bâtiment A, 31000, Toulouse, France.

The horse was essential to past human societies but became a recreational animal during the twentieth century as the world became increasingly mechanized. As the author reviews here, recent studies of ancient genomes have revisited the understanding of horse domestication, from the very early stages to the most modern developments. They have uncovered several extinct lineages roaming the far ends of Eurasia some 4000 years ago. They have shown that the domestic horse has been significantly reshaped during the last millennium and experienced a sharp decline in genetic diversity within the last two centuries. At a time when no truly wild horses exist any longer, this calls for enhanced conservation in all endangered populations. These include the Przewalski's horse native to Mongolia, and the many local breeds side-lined by the modern agenda, but yet representing the living heritage of over five millennia of horse breeding.
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http://dx.doi.org/10.1002/bies.201900164DOI Listing
January 2020

Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny.

Nature 2019 10 11;574(7776):103-107. Epub 2019 Sep 11.

Evolutionary Genomics Section, Globe Institute, University of Copenhagen, Copenhagen, Denmark.

The sequencing of ancient DNA has enabled the reconstruction of speciation, migration and admixture events for extinct taxa. However, the irreversible post-mortem degradation of ancient DNA has so far limited its recovery-outside permafrost areas-to specimens that are not older than approximately 0.5 million years (Myr). By contrast, tandem mass spectrometry has enabled the sequencing of approximately 1.5-Myr-old collagen type I, and suggested the presence of protein residues in fossils of the Cretaceous period-although with limited phylogenetic use. In the absence of molecular evidence, the speciation of several extinct species of the Early and Middle Pleistocene epoch remains contentious. Here we address the phylogenetic relationships of the Eurasian Rhinocerotidae of the Pleistocene epoch, using the proteome of dental enamel from a Stephanorhinus tooth that is approximately 1.77-Myr old, recovered from the archaeological site of Dmanisi (South Caucasus, Georgia). Molecular phylogenetic analyses place this Stephanorhinus as a sister group to the clade formed by the woolly rhinoceros (Coelodonta antiquitatis) and Merck's rhinoceros (Stephanorhinus kirchbergensis). We show that Coelodonta evolved from an early Stephanorhinus lineage, and that this latter genus includes at least two distinct evolutionary lines. The genus Stephanorhinus is therefore currently paraphyletic, and its systematic revision is needed. We demonstrate that sequencing the proteome of Early Pleistocene dental enamel overcomes the limitations of phylogenetic inference based on ancient collagen or DNA. Our approach also provides additional information about the sex and taxonomic assignment of other specimens from Dmanisi. Our findings reveal that proteomic investigation of ancient dental enamel-which is the hardest tissue in vertebrates, and is highly abundant in the fossil record-can push the reconstruction of molecular evolution further back into the Early Pleistocene epoch, beyond the currently known limits of ancient DNA preservation.
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http://dx.doi.org/10.1038/s41586-019-1555-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6894936PMC
October 2019

Origin and Evolution of Deleterious Mutations in Horses.

Genes (Basel) 2019 08 28;10(9). Epub 2019 Aug 28.

Laboratoire d'Anthropobiologie Moléculaire et d'Imagerie de Synthèse, CNRS UMR 5288, Université de Toulouse, Université Paul Sabatier, 31000 Toulouse, France.

Domestication has changed the natural evolutionary trajectory of horses by favoring the reproduction of a limited number of animals showing traits of interest. Reduced breeding stocks hampered the elimination of deleterious variants by means of negative selection, ultimately inflating mutational loads. However, ancient genomics revealed that mutational loads remained steady during most of the domestication history until a sudden burst took place some 250 years ago. To identify the factors underlying this trajectory, we gather an extensive dataset consisting of 175 modern and 153 ancient genomes previously published, and carry out the most comprehensive characterization of deleterious mutations in horses. We confirm that deleterious variants segregated at low frequencies during the last 3500 years, and only spread and incremented their occurrence in the homozygous state during modern times, owing to inbreeding. This independently happened in multiple breeds, following both the development of closed studs and purebred lines, and the deprecation of horsepower in the 20th century, which brought many draft breeds close to extinction. Our work illustrates the paradoxical effect of some conservation and improvement programs, which reduced the overall genomic fitness and viability.
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http://dx.doi.org/10.3390/genes10090649DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6769756PMC
August 2019

EPAS1 gain-of-function mutation contributes to high-altitude adaptation in Tibetan horses.

Mol Biol Evol 2019 Jul 2. Epub 2019 Jul 2.

Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, P. R. China.

High altitude represents some of the most extreme environments worldwide. The genetic changes underlying adaptation to such environments have been recently identified in multiple animals but remain unknown in horses. Here, we sequence the complete genome of 138 domestic horses encompassing a whole altitudinal range across China to uncover the genetic basis for adaptation to high-altitude hypoxia. Our genome dataset includes 65 lowland animals across ten Chinese native breeds, 61 horses living at least 3,300 meters above sea level across seven locations along Qinghai-Tibet Plateau, as well as 7 Thoroughbred and 5 Przewalski's horses added for comparison. We find that Tibetan horses do not descend from Przewalski's horses but were most likely introduced from a distinct horse lineage, following the emergence of pastoral nomadism in Northwestern China ∼3,700 years ago. We identify that the endothelial PAS domain protein 1 gene (EPAS1, alsoHIF2A) shows the strongest signature for positive selection in the Tibetan horse genome. Two missense mutations at this locus appear strongly associated with blood physiological parameters facilitating blood circulation as well as oxygen transportation and consumption in hypoxic conditions. Functional validation through protein mutagenesis shows that these mutations increase EPAS1 stability and its hetero dimerization affinity to ARNT (HIF1B). Our study demonstrates that missense mutations in the EPAS1 gene provided key evolutionary molecular adaptation to Tibetan horses living in high-altitude hypoxic environments. It reveals possible targets for genomic selection programs aimed at increasing hypoxia tolerance in livestock and provides a textbook example of evolutionary convergence across independent mammal lineages.
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http://dx.doi.org/10.1093/molbev/msz158DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6805228PMC
July 2019

Joint Estimates of Heterozygosity and Runs of Homozygosity for Modern and Ancient Samples.

Genetics 2019 07 14;212(3):587-614. Epub 2019 May 14.

Lundbeck Foundation GeoGenetics Center, Globe Institute, University of Copenhagen, 1350K, Denmark.

Both the total amount and the distribution of heterozygous sites within individual genomes are informative about the genetic diversity of the population they belong to. Detecting true heterozygous sites in ancient genomes is complicated by the generally limited coverage achieved and the presence of post-mortem damage inflating sequencing errors. Additionally, large runs of homozygosity found in the genomes of particularly inbred individuals and of domestic animals can skew estimates of genome-wide heterozygosity rates. Current computational tools aimed at estimating runs of homozygosity and genome-wide heterozygosity levels are generally sensitive to such limitations. Here, we introduce ROHan, a probabilistic method which substantially improves the estimate of heterozygosity rates both genome-wide and for genomic local windows. It combines a local Bayesian model and a Hidden Markov Model at the genome-wide level and can work both on modern and ancient samples. We show that our algorithm outperforms currently available methods for predicting heterozygosity rates for ancient samples. Specifically, ROHan can delineate large runs of homozygosity (at megabase scales) and produce a reliable confidence interval for the genome-wide rate of heterozygosity outside of such regions from modern genomes with a depth of coverage as low as 5-6× and down to 7-8× for ancient samples showing moderate DNA damage. We apply ROHan to a series of modern and ancient genomes previously published and revise available estimates of heterozygosity for humans, chimpanzees and horses.
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http://dx.doi.org/10.1534/genetics.119.302057DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6614887PMC
July 2019

Tracking Five Millennia of Horse Management with Extensive Ancient Genome Time Series.

Cell 2019 05 2;177(6):1419-1435.e31. Epub 2019 May 2.

Lundbeck Foundation GeoGenetics Center, University of Copenhagen, 1350K Copenhagen, Denmark.

Horse domestication revolutionized warfare and accelerated travel, trade, and the geographic expansion of languages. Here, we present the largest DNA time series for a non-human organism to date, including genome-scale data from 149 ancient animals and 129 ancient genomes (≥1-fold coverage), 87 of which are new. This extensive dataset allows us to assess the modern legacy of past equestrian civilizations. We find that two extinct horse lineages existed during early domestication, one at the far western (Iberia) and the other at the far eastern range (Siberia) of Eurasia. None of these contributed significantly to modern diversity. We show that the influence of Persian-related horse lineages increased following the Islamic conquests in Europe and Asia. Multiple alleles associated with elite-racing, including at the MSTN "speed gene," only rose in popularity within the last millennium. Finally, the development of modern breeding impacted genetic diversity more dramatically than the previous millennia of human management.
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http://dx.doi.org/10.1016/j.cell.2019.03.049DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6547883PMC
May 2019

DamMet: ancient methylome mapping accounting for errors, true variants, and post-mortem DNA damage.

Gigascience 2019 04;8(4)

Lundbeck Foundation GeoGenetics Center, University of Copenhagen, Øster Voldgade 5-7, 1350K Copenhagen, Denmark.

Background: Recent computational advances in ancient DNA research have opened access to the detection of ancient DNA methylation footprints at the genome-wide scale. The most commonly used approach infers the methylation state of a given genomic region on the basis of the amount of nucleotide mis-incorporations observed at CpG dinucleotide sites. However, this approach overlooks a number of confounding factors, including the presence of sequencing errors and true variants. The scale and distribution of the inferred methylation measurements are also variable across samples, precluding direct comparisons.

Findings: Here, we present DamMet, an open-source software program retrieving maximum likelihood estimates of regional CpG methylation levels from ancient DNA sequencing data. It builds on a novel statistical model of post-mortem DNA damage for dinucleotides, accounting for sequencing errors, genotypes, and differential post-mortem cytosine deamination rates at both methylated and unmethylated sites. To validate DamMet, we extended gargammel, a sequence simulator for ancient DNA data, by introducing methylation-dependent features of post-mortem DNA decay. This new simulator provides direct validation of DamMet predictions. Additionally, the methylation levels inferred by DamMet were found to be correlated to those inferred by epiPALEOMIX and both on par and directly comparable to those measured from whole-genome bisulphite sequencing experiments of fresh tissues.

Conclusions: DamMet provides genuine estimates for local DNA methylation levels in ancient individual genomes. The returned estimates are directly cross-sample comparable, and the software is available as an open-source C++ program hosted at https://gitlab.com/KHanghoj/DamMet along with a manual and tutorial.
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http://dx.doi.org/10.1093/gigascience/giz025DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6474913PMC
April 2019

Authentication and Assessment of Contamination in Ancient DNA.

Methods Mol Biol 2019 ;1963:163-194

Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen K, Denmark.

Contamination from both present-day humans and postmortem microbial sources is a common challenge in ancient DNA studies. Here we present a suite of tools to assist in the assessment of contamination in ancient DNA data sets. These tools perform standard tests of authenticity of ancient DNA data including detecting the presence of postmortem damage signatures in sequence alignments and quantifying the amount of present-day human contamination.
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http://dx.doi.org/10.1007/978-1-4939-9176-1_17DOI Listing
September 2019

Paleogenomics: reconstruction of plant evolutionary trajectories from modern and ancient DNA.

Genome Biol 2019 02 11;20(1):29. Epub 2019 Feb 11.

INRA-UCA UMR 1095 Génétique Diversité et Ecophysiologie des Céréales, 63100, Clermont-Ferrand, France.

How contemporary plant genomes originated and evolved is a fascinating question. One approach uses reference genomes from extant species to reconstruct the sequence and structure of their common ancestors over deep timescales. A second approach focuses on the direct identification of genomic changes at a shorter timescale by sequencing ancient DNA preserved in subfossil remains. Merged within the nascent field of paleogenomics, these complementary approaches provide insights into the evolutionary forces that shaped the organization and regulation of modern genomes and open novel perspectives in fostering genetic gain in breeding programs and establishing tools to predict future population changes in response to anthropogenic pressure and global warming.
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http://dx.doi.org/10.1186/s13059-019-1627-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6369560PMC
February 2019
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