Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe

Domestication; Evolution; Gene flow; Neolithic; Article; DNA sequence; Europe; European wild boar; Middle East; Animals; DNA, Ancient; DNA, Mitochondrial; History, Ancient; Phylogeny; Skin Pigmentation; Swine

Abstract :

[en] Archaeological evidence indicates that pig domestication had begun by ∼10,500 y before the present (BP) in the Near East, and mitochondrial DNA (mtDNA) suggests that pigs arrived in Europe alongside farmers ∼8,500 y BP. A few thousand years after the introduction of Near Eastern pigs into Europe, however, their characteristic mtDNA signature disappeared and was replaced by haplotypes associated with European wild boars. This turnover could be accounted for by substantial gene flow from local European wild boars, although it is also possible that European wild boars were domesticated independently without any genetic contribution from the Near East. To test these hypotheses, we obtained mtDNA sequences from 2,099 modern and ancient pig samples and 63 nuclear ancient genomes from Near Eastern and European pigs. Our analyses revealed that European domestic pigs dating from 7,100 to 6,000 y BP possessed both Near Eastern and European nuclear ancestry, while later pigs possessed no more than 4% Near Eastern ancestry, indicating that gene flow from European wild boars resulted in a near-complete disappearance of Near East ancestry. In addition, we demonstrate that a variant at a locus encoding black coat color likely originated in the Near East and persisted in European pigs. Altogether, our results indicate that while pigs were not independently domesticated in Europe, the vast majority of human-mediated selection over the past 5,000 y focused on the genomic fraction derived from the European wild boars, and not on the fraction that was selected by early Neolithic farmers over the first 2,500 y of the domestication process. © 2019 National Academy of Sciences. All rights reserved.

Disciplines :

Veterinary medicine & animal health
Archaeology

Author, co-author :

Frantz, L. A. F.; School of Biological and Chemical Sciences, Queen Mary University of London, London, E1 4NS, United Kingdom, Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, OX1 3TG, United Kingdom

Haile, J.; Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, OX1 3TG, United Kingdom

Lin, A. T.; Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, OX1 3TG, United Kingdom, Department of Zoology, University of Oxford, Oxford, OX1 3SZ, United Kingdom

Scheu, A.; Palaeogenetics Group, Institute of Organismic and Molecular Evolution, Johannes Gutenberg-University Mainz, Mainz, D-55128, Germany

Geörg, C.; Palaeogenetics Group, Institute of Organismic and Molecular Evolution, Johannes Gutenberg-University Mainz, Mainz, D-55128, Germany

Benecke, N.; Department of Natural Sciences, German Archaeological Institute, Berlin, 14195, Germany

Alexander, M.; BioArCh, Department of Archaeology, University of York, York, YO10 5NG, United Kingdom

Linderholm, A.; Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, OX1 3TG, United Kingdom, Department of Anthropology, Texas AandM University, College Station, TX 77840, United States

Mullin, V. E.; Department of Earth Sciences, Natural History Museum, London, SW7 5BD, United Kingdom, Molecular Population Genetics, Smurfit Institute of Genetics, Trinity College Dublin, Dublin 2, Ireland

Daly, K. G.; Department of Anthropology, University of Michigan, Ann Arbor, MI 48109, United States

More authors (90 more)

Language :

English

Title :

Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe

Publication date :

2019

Journal title :

Proceedings of the National Academy of Sciences of the United States of America

ISSN :

0027-8424

eISSN :

1091-6490

Publisher :

National Academy of Sciences, Washington DC, United States - District of Columbia

Volume :

116

Issue :

Pages :

17231-17238

Peer reviewed :

Peer Reviewed verified by ORBi

Funding text :

Autoritatea NationalÄ pentru Cercetare StiintificÄ : PN‐III-P4‐ID‐PCE‐2016‐0676Ministarstvo Prosvete, Nauke i TehnoloÅ¡kog Razvoja, MPNTR: III 47001, BCS-0530699, BCS-1311551American Research Institute in Turkey, ARITWellcome Trust, WT: 210119/Z/18/ZERC-2013-CoG-614725–PATHPHYLODYNMinisterio de EconomÃa y Competitividad, MINECOUniversity of Oxford: ERC-2013-StG-337574-UNDEADDeutsche Forschungsgemeinschaft, DFG: PE 424/10,1-3, CGL2015-65387-C3-2-P MINECO-FEDERPN-II-RU-TE-2012-3-0461Instituto Nacional de CiÃªncia e Tecnologia para Excitotoxicidade e NeuroproteÃ§Ã£o, INCT-EN: SFRH/BPD/ 108326/2015National Science Foundation, NSF: 1119354, 1202692, 0527732, 0638897, 0629500, 1446308, 0732327, 1203823, 1203268, 1249313, 0947862, 1140106National Geographic Society, NGSIcelandic Centre for Research, RANNISNarodowe Centrum Nauki, NCN: 2017/25/B/HS3/01242NE/K005243/1, ERC-2015-CoG-681396, 295729-CodeX, NE/K003259/1Junta de Castilla y LeÃ³nSG143331

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Bibliography

M. A. Zeder, "Out of the fertile crescent: The dispersal of domestic livestock through Europe and Africa" in Human Dispersal and Species Movement: From Prehistory to the Present, N. Boivin, R. Crassard, M. Petraglia, Eds. (Cambridge University Press, 2017), pp. 261-303.
Z. Hofmanová et al., Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl. Acad. Sci. U.S.A. 113, 6886-6891 (2016).
J. Conolly et al., Meta-analysis of zooarchaeological data from SW Asia and SE Europe provides insight into the origins and spread of animal husbandry. J. Archaeol. Sci. 38, 538-545 (2011).
J. Peters, A. von den Driesch, D. Helmer, "The Upper Euphrates-Tigris Basin: Cradle of agro-pastoralism?" in The First Steps of Animal Domestication: New Archaeozoological Approaches. Proceedings of the Ninth International Council of Archeozoology, J.D. Vigne, J. Peters, D. Helmer, Eds. (Oxbow Books, Oxford, 2005), pp. 96-123.
K. G. Daly et al., Ancient goat genomes reveal mosaic domestication in the Fertile Crescent. Science 361, 85-88 (2018).
S. Colledge, J. Conolly, K. Dobney, K. Manning, S. Shennan, Origins and Spread of Domestic Animals in Southwest Asia and Europe (Left Coast Press, 2013).
L. Frantz et al., The evolution of Suidae. Annu. Rev. Anim. Biosci. 4, 61-85 (2016).
P. Rowley-Conwy, U. Albarella, K. Dobney, Distinguishing wild boar from domestic pigs in prehistory: A review of approaches and recent results. J. World Prehist. 25, 1-44 (2012).
X. Lemoine, M. A. Zeder, K. J. Bishop, S. J. Rufolo, A new system for computing dentition-based age profiles in Sus scrofa. J. Archaeol. Sci. 47, 179-193 (2014).
M. A. Zeder, Core questions in domestication research. Proc. Natl. Acad. Sci. U.S.A. 112, 3191-3198 (2015).
A. Evin et al., The long and winding road: Identifying pig domestication through molar size and shape. J. Archaeol. Sci. 40, 735-743 (2013).
T. Cucchi, A. Hulme-Beaman, J. Yuan, K. Dobney, Early Neolithic pig domestication at Jiahu, Henan Province, China: Clues from molar shape analyses using geometric morphometric approaches. J. Archaeol. Sci. 38, 11-22 (2011).
M. Balasse, et al., "Wild game or farm animal? Tracking human-pig relationships in ancient times through stable isotope analysis" in Hybrid Communities Biosocial Approaches to Domestication and Other Trans-species Relationships, C. Stépanoff, J.-D. Vigne, Eds. (Routledge Studies in Anthropology, Routledge, Abingdon, Oxon, UK, ed. 1, 2018), pp. 81-96.
A. Dinu, A. Boroneant, A. Balasescu, A. Soficaru, D. Miritoiu, Mesolithic and Neolithic pigs of the northern Balkans: Astragali vs. teeth as markers of domestication. Mesolithic Miscellany 19, 7-12 (2008).
A. Legge, Practice with science: Molar tooth eruption ages in domestic, feral and wild pigs (Sus scrofa). Int. J. Osteoarchaeol. (2013) https://onlinelibrary.wiley.com/page/journal/10991212/homepage/News.html. Accessed 25 July 2019.
A. J. Legge, "Bone measurements and body weights from some Australian feral pigs" in Economic Zooarchaeology: Studies in Hunting, Herding and Early Agriculture, P. Rowley-Conwy, D. Sergeantson, P. Halstead, Eds. (Oxbow Books, Oxford, ed. 1, 2017).
S. Payne, G. Bull, Components of variation in measurements of pig bones and teeth, and the use of measurements to distinguish wild from domestic pig remains. Archaeozoologia 2, 27-65 (1988).
C. Lega, P. Raia, L. Rook, D. Fulgione, Size matters: A comparative analysis of pig domestication. Holocene 26, 327-332 (2016).
A. Evin et al., Unravelling the complexity of domestication: A case study using morphometrics and ancient DNA analyses of archaeological pigs from Romania. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20130616 (2015).
A. Evin et al., Phenotype and animal domestication: A study of dental variation between domestic, wild, captive, hybrid and insular Sus scrofa. BMC Evol. Biol. 15, 6 (2015).
G. Larson et al., Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proc. Natl. Acad. Sci. U.S.A. 104, 15276-15281 (2007).
A. Manunza et al., A high throughput genotyping approach reveals distinctive autosomal genetic signatures for European and Near Eastern wild boar. PLoS One 8, e55891 (2013).
K. J. Gron, L. Sørensen, Cultural and economic negotiation: A new perspective on the Neolithic transition of Southern Scandinavia. Antiquity 92, 958-974 (2018).
P. Sillitoe, "Pigs in the New Guinea Highlands: An ethnographic example" in Pigs and Humans: 10,000 Years of Interaction, U. Albarella, K. Dobney, A. Ervynck, Eds. (Oxford University Press, Oxford, UK, 2007), vol. 10, pp. 330-356.
J. Studer, D. Pillonel, "Traditional pig butchery by the Yali people of West Papua (Irian Jaya): An ethnographic and archaeozoological example" in Pigs and Humans: 10,000 Years of Interaction, U. Albarella, K. Dobney, A. Ervynck, Eds. (Oxford University Press, Oxford, UK, 2007), pp. 308-329.
L. A. F. Frantz et al., Evidence of long-term gene flow and selection during domestication from analyses of Eurasian wild and domestic pig genomes. Nat. Genet. 47, 1141-1148 (2015).
S. Vai et al., The Biarzo case in northern Italy: Is the temporal dynamic of swine mitochondrial DNA lineages in Europe related to domestication? Sci. Rep. 5, 16514 (2015).
C. Ottoni et al., Pig domestication and human-mediated dispersal in western Eurasia revealed through ancient DNA and geometric morphometrics. Mol. Biol. Evol. 30, 824-832 (2013).
C. Lega et al., Like a pig out of water: Seaborne spread of domestic pigs in Southern Italy and Sardinia during the Bronze and iron ages. Heredity 118, 154-159 (2017).
B. Chessa et al., Revealing the history of sheep domestication using retrovirus integrations. Science 324, 532-536 (2009).
W. Haak et al., Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207-211 (2015).
G. Larson et al., Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 307, 1618-1621 (2005).
B. Krause-Kyora et al., Use of domesticated pigs by Mesolithic hunter-gatherers in northwestern Europe. Nat. Commun. 4, 2348 (2013).
G. Hellenthal et al., A genetic atlas of human admixture history. Science 343, 747-751 (2014).
S. White, From globalized pig breeds to capitalist pigs: A study in animal cultures and evolutionary history. Environ. Hist. Durh. N. C. 16, 94-120 (2011).
M. Bosse et al., Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression. Nat. Commun. 5, 4392 (2014).
V. Maselli et al., Southern Italian wild boar population, hotspot of genetic diversity. Hystrix It. J. Mammal, 10.4404/hystrix-27.2-1148927 (2016).
D. H. Alexander, J. Novembre, K. Lange, Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664 (2009).
O. Delaneau, J. Marchini, J.-F. Zagury, A linear complexity phasing method for thousands of genomes. Nat. Methods 9, 179-181 (2011).
M. Fang, G. Larson, H. S. Ribeiro, N. Li, L. Andersson, Contrasting mode of evolution at a coat color locus in wild and domestic pigs. PLoS Genet. 5, e1000341 (2009).
D. J. Goedbloed et al., Genome-wide single nucleotide polymorphism analysis reveals recent genetic introgression from domestic pigs into Northwest European wild boar populations. Mol. Ecol. 22, 856-866 (2013).
U. Albarella, F. Manconi, A. Trentacoste, "A week on the plateau: Pig husbandry, mobility and resource exploitation in central Sardinia" in Ethnozooarchaeology. The Present and Past of Human-Animal Relationships, U. Albarella, A. Trentacoste, Eds. (Oxbow Books, Oxford, 2011), pp. 143-159.
A. Hadjikoumis, "The origins and evolution of pig domestication in prehistoric Spain" PhD thesis, University of Sheffield, Sheffield, UK (2010). http://etheses.whiterose.ac.uk/23773/. Accessed 16 May 2019.
P. Halstead, V. Isaakidou, "A Pig Fed by Hand is Worth Two in the Bush" in Ethnozooarchaeology: The Present and Past of Human-Animal Relationships, U. Albarella, A. Trentacoste, Eds. (Oxbow Books, Oxford, 2011), pp. 160-174.
M. MacKinnon, High on the hog: Linking zooarchaeological, literary, and artistic data for pig breeds in Roman Italy. Am. J. Archaeol. 105, 649-673 (2001).
M. Currat, M. Ruedi, R. J. Petit, L. Excoffier, The hidden side of invasions: Massive introgression by local genes. Evolution 62, 1908-1920 (2008).
G. Larson, J. Burger, A population genetics view of animal domestication. Trends Genet. 29, 197-205 (2013).
L. A. F. Frantz, G. Larson, "A genetic perspective on the domestication continuum" in Hybrid Communities, C. Stépanoff, J.-D. Vigne, Eds. (Routledge Studies in Anthropology, Routledge, Abingdon, Oxon, UK, ed. 1, 2018), vol. 46, pp 23-37.
S. D. E. Park et al., Genome sequencing of the extinct Eurasian wild aurochs, Bos primigenius, illuminates the phylogeography and evolution of cattle. Genome Biol. 16, 234 (2015).
V. Warmuth et al., Reconstructing the origin and spread of horse domestication in the Eurasian steppe. Proc. Natl. Acad. Sci. U.S.A. 109, 8202-8206 (2012).
M. Ní Leathlobhair et al., The evolutionary history of dogs in the Americas. Science 361, 81-85 (2018).
J. Eriksson et al., Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken. PLoS Genet. 4, e1000010 (2008).
S. Myles et al., Genetic structure and domestication history of the grape. Proc. Natl. Acad. Sci. U.S.A. 108, 3530-3535 (2011).
A. Cornille et al., New insight into the history of domesticated apple: Secondary contribution of the European wild apple to the genome of cultivated varieties. PLoS Genet. 8, e1002703 (2012).
L. Kistler et al., Multiproxy evidence highlights a complex evolutionary legacy of maize in South America. Science 362, 1309-1313 (2018).
R. R. da Fonseca et al., The origin and evolution of maize in the Southwestern United States. Nat. Plants 1, 14003 (2015).