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. 2019 Aug 27;116(35):17231-17238.
doi: 10.1073/pnas.1901169116. Epub 2019 Aug 12.

Ancient Pigs Reveal a Near-Complete Genomic Turnover Following Their Introduction to Europe

Laurent A F Frantz  1   2 James Haile  2 Audrey T Lin  2   3 Amelie Scheu  4 Christina Geörg  4 Norbert Benecke  5 Michelle Alexander  6 Anna Linderholm  2   7 Victoria E Mullin  8   9 Kevin G Daly  9 Vincent M Battista  10 Max Price  11 Kurt J Gron  12 Panoraia Alexandri  13 Rose-Marie Arbogast  14 Benjamin Arbuckle  15 Adrian Bӑlӑşescu  16 Ross Barnett  12 László Bartosiewicz  17 Gennady Baryshnikov  18 Clive Bonsall  19 Dušan Borić  20 Adina Boroneanţ  16 Jelena Bulatović  21 Canan Çakirlar  22 José-Miguel Carretero  23 John Chapman  12 Mike Church  12 Richard Crooijmans  24 Bea De Cupere  25 Cleia Detry  26 Vesna Dimitrijevic  21 Valentin Dumitraşcu  16 Louis du Plessis  3 Ceiridwen J Edwards  27 Cevdet Merih Erek  28 Aslı Erim-Özdoğan  29 Anton Ervynck  30 Domenico Fulgione  31 Mihai Gligor  32 Anders Götherström  33 Lionel Gourichon  34 Martien A M Groenen  24 Daniel Helmer  35 Hitomi Hongo  36 Liora K Horwitz  37 Evan K Irving-Pease  2 Ophélie Lebrasseur  2   38 Joséphine Lesur  39 Caroline Malone  40 Ninna Manaseryan  41 Arkadiusz Marciniak  42 Holley Martlew  43 Marjan Mashkour  39 Roger Matthews  44 Giedre Motuzaite Matuzeviciute  45 Sepideh Maziar  46 Erik Meijaard  47   48   49 Tom McGovern  50 Hendrik-Jan Megens  24 Rebecca Miller  51 Azadeh Fatemeh Mohaseb  39 Jörg Orschiedt  52   53 David Orton  6 Anastasia Papathanasiou  54 Mike Parker Pearson  55 Ron Pinhasi  56 Darko Radmanović  57 François-Xavier Ricaut  58 Mike Richards  59 Richard Sabin  60 Lucia Sarti  61 Wolfram Schier  52 Shiva Sheikhi  39 Elisabeth Stephan  62 John R Stewart  63 Simon Stoddart  64 Antonio Tagliacozzo  65 Nenad Tasić  66 Katerina Trantalidou  54 Anne Tresset  39 Cristina Valdiosera  67 Youri van den Hurk  22 Sophie Van Poucke  25 Jean-Denis Vigne  39 Alexander Yanevich  68 Andrea Zeeb-Lanz  69 Alexandros Triantafyllidis  13 M Thomas P Gilbert  70   71 Jörg Schibler  72 Peter Rowley-Conwy  12 Melinda Zeder  73 Joris Peters  74   75 Thomas Cucchi  39 Daniel G Bradley  9 Keith Dobney  38   59   76 Joachim Burger  4 Allowen Evin  77 Linus Girdland-Flink  78 Greger Larson  79
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Free PMC article

Ancient Pigs Reveal a Near-Complete Genomic Turnover Following Their Introduction to Europe

Laurent A F Frantz et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

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.

Keywords: Neolithic; domestication; evolution; gene flow.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
(A) Map representing the distribution of East Asian (blue), Near Eastern (including haplogroups mt-Y1 and mt-ArmT; yellow), European (including haplogroups mt-Italian, mt-A, mt-C, and mt-Y2; red), and Y2 (purple) haplogroups in wild boars. Black dots represent the locations of 696 modern and ancient wild boar. Haplogroup assignments were used to interpolate the underlying color distribution, which demonstrates the biogeographical boundaries of these 3 general haplogroups. (B) Large pie chart in the upper right corner of the map represents overall frequencies of these haplogroups in domestic pigs. Small pie charts on the map show the frequencies at various archeological sites/locations between 8,000 y BP and 5,100 y BP (B), between 5,099 and 180 y BP [before the Industrial Revolution and the introduction of Asian pigs in Europe (35) (C), and in modern pigs (D)]. A few samples from our datasets have been excluded from these plots; more details are provided in SI Appendix, Figs. S6 and S7.
Fig. 2.
Fig. 2.
(A) Bar plots representing the proportion of ancestry from Europe (red), the Near East (yellow), and East Asia (blue) in Eurasian wild boar genomes. (B) Bar plots depicting the proportion of Near Eastern ancestry in modern and ancient European domestic pigs. (C) PCA (excluding East Asian domestic pigs; SI Appendix, Fig. S14) showing the existence of 2 groups of ancient domestic pigs: 1 close to Near Eastern wild boar and 1 close to European wild boar.

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