Evidence of long-term gene flow and selection during domestication from analyses of Eurasian wild and domestic pig genomes

Nature Genetics

Volumn 47, Issue 10, 2015, Pages 1141-1148

  Frantz, Laurent A F ^a,b   Schraiber, Joshua G ^c,d   Madsen, Ole ^a   Megens, Hendrik Jan ^a   Cagan, Alex ^e   Bosse, Mirte ^a   Paudel, Yogesh ^a   Crooijmans, Richard P M A ^a   Larson, Greger ^b   Groenen, Martien A M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ASIA; BOTTLENECK POPULATION; DOMESTIC PIG; DOMESTICATION; EUROPE; GENE FLOW; GENE LOCUS; GENE SEQUENCE; GENETIC SELECTION; GENETIC TRAIT; GENOME ANALYSIS; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; RECURRENT SELECTION; REPRODUCTIVE ISOLATION; WILD BOAR; ANIMAL; DOMESTIC ANIMAL; GENETICS; GENOME; PIG; WILD ANIMAL;

ANIMALS; ANIMALS, DOMESTIC; ANIMALS, WILD; ASIA; EUROPE; GENE FLOW; GENOME; SWINE;

EID: 84942985288     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3394     Document Type: Article

References (86)

1. Childe V.G. The Dawn of European Civilization 6th edn. (Routledge, & Kegan Paul, 1968
2. Darwin C. The Variation of Animals and Plants Under Domestication (John Murray, 1868
3. Price E.O. Animal Domestication and Behavior (CABI Publishing, 2002
4. Driscoll C.A., Macdonald D.W., & OBrien S.J. From wild animals to domestic pets, an evolutionary view of domestication. Proc. Natl. Acad. Sci. USA 106, 9971-9978 (2009
5. OConnor T.P. Wild or domestic?. Biometric variation in the cat Felis silvestris Schreber. Int. J. Osteoarchaeol. 17, 581-595 (2007
6. Larson G., et al. Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 307, 1618-1621 (2005
7. Hanotte O., et al. African pastoralism: genetic imprints of origins and migrations. Science 296, 336-339 (2002
8. Luikart G., et al. Multiple maternal origins and weak phylogeographic structure in domestic goats. Proc. Natl. Acad. Sci. USA 98, 5927-5932 (2001
9. Naderi S., et al. The goat domestication process inferred from large-scale mitochondrial DNA analysis of wild and domestic individuals. Proc. Natl. Acad. Sci. USA 105, 17659-17664 (2008
10. Pedrosa S., et al. Evidence of three maternal lineages in Near Eastern sheep supporting multiple domestication events. Proc. Biol. Sci. 272, 2211-2217 (2005
11. Vilà C., et al. Widespread origins of domestic horse lineages. Science 291, 474-477 (2001
12. Larson G., & Fuller D.Q. The evolution of animal domestication. Annu. Rev. Ecol. Evol. Syst. 45, 115-136 (2014
13. Zeder M.A. Domestication and early agriculture in the Mediterranean Basin: origins, diffusion, and impact. Proc. Natl. Acad. Sci. USA 105, 11597-11604 (University of Oklahoma Press, 2008
14. Macneish R.S. The Origins of Agriculture and Settled Life (University of Oklahoma Press, 1992
15. Zeder M.A. in Harlan II: Biodiversity in Agriculture: Domestication, Evolution and Sustainability (eds. Damania A., & Gepts P.) 227-229 (Univ. California Press, 2011
16. Vigne J.-D. The origins of animal domestication and husbandry: a major change in the history of humanity and the biosphere. C. R. Biol. 334, 171-181 (2011
17. Dobney K., & Larson G. Genetics and animal domestication: new windows on an elusive process. J. Zool. (Lond.) 269, 261-271 (2006
18. Marshall F.B., Dobney K., Denham T., & Capriles J.M. Evaluating the roles of directed breeding and gene flow in animal domestication. Proc. Natl. Acad. Sci. USA 111, 6153-6158 (2014
19. Ervynck A., Hongo H., Dobney K., & Meadow R. Born free?. New evidence for the status of Sus scrofa at Neolithic Çayönü Tepesi (Southeastern Anatolia, Turkey). Paléorient 27, 47-73 (2001
20. Cucchi T., Hulme-Beaman A., Yuan J., & Dobney K. 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
21. Larson G., et al. Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proc. Natl. Acad. Sci. USA 104, 15276-15281 (2007
22. Ottoni C., 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
23. Albarella U., Manconi F., & Trentacoste A. in Ethnozooarchaeology. The Present and Past of Human-Animal Relationships (eds. Albarella U., & Trentacoste A.) 143-159 (Oxbow Books, 2011
24. White S. From globalized pig breeds to capitalist pigs: a study in animal cultures and evolutionary history. Environ. Hist. 16, 94-120 (2011
25. Evin A., et al. The long and winding road: identifying pig domestication through molar size and shape. J. Archaeol. Sci. 40, 735-743 (2013
26. Albarella U., Davis S.J.M., Detry C.P., & Rowley-Conwy P. Pigs of the Far West: the biometry of Sus from archaeological sites in Portugal. Anthropozoologica 40, 27-54 (2005
27. Rowley-Conwy P., Albarella U., & Dobney K. Distinguishing wild boar from domestic pigs in prehistory: a review of approaches and recent results. J. World Prehist. 25, 1-44 (2012
28. Owen J., et al. The zooarchaeological application of quantifying cranial shape differences in wild boar and domestic pigs (Sus scrofa) using 3D geometric morphometrics. J. Archaeol. Sci. 43, 159-167 (2014
29. Porter V. Pigs: A Handbook to the Breeds of the World (Helm Information, 1993
30. Groenen M.A.M., et al. Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491, 393-398 (2012
31. Bosse M., et al. Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression. Nat. Commun. 5, 4392 (2014
32. Bosse M., et al. Untangling the hybrid nature of modern pig genomes: a mosaic derived from biogeographically distinct and highly divergent Sus scrofa populations. Mol. Ecol. 23, 4089-4102 (2014
33. Frantz L.A., et al. Genome sequencing reveals fine scale diversification and reticulation history during speciation in Sus. Genome Biol. 14, R107 (2013
34. Bosse M., et al. Regions of homozygosity in the porcine genome: consequence of demography and the recombination landscape. PLoS Genet. 8, e1003100 (2012
35. Frantz L.A.F., Madsen O., Megens H.-J., Groenen M.A.M., & Lohse K. Testing models of speciation from genome sequences: divergence and asymmetric admixture in Island Southeast Asian Sus species during the Plio-Pleistocene climatic fluctuations. Mol. Ecol. 23, 5566-5574 (2014
36. Ai H., et al. Adaptation and possible ancient interspecies introgression in pigs identified by whole-genome sequencing. Nat. Genet. 47, 217-225 (2015
37. Nielsen R., et al. Genomic scans for selective sweeps using SNP data. Genome Res. 15, 1566-1575 (2005
38. Pavlidis P., Živkovic D., Stamatakis A., & Alachiotis N. SweeD: likelihood-based detection of selective sweeps in thousands of genomes. Mol. Biol. Evol. 30, 2224-2234 (2013
39. Huber C.D., Nordborg M., Hermisson J., & Hellmann I. Keeping it local: evidence for positive selection in Swedish Arabidopsis thaliana. Mol. Biol. Evol. 31, 3026-3039 (2014
40. Andersson-Eklund L., et al. Mapping quantitative trait loci for carcass and meat quality traits in a wild boar × Large White intercross. J. Anim. Sci. 76, 694-700 (1998
41. Rubin C.-J., et al. Strong signatures of selection in the domestic pig genome. Proc. Natl. Acad. Sci. USA 109, 19529-19536 (2012
42. Karim L., et al. Variants modulating the expression of a chromosome domain encompassing PLAG1 influence bovine stature. Nat. Genet. 43, 405-413 (2011
43. Setoguchi K., et al. Cross-breed comparisons identified a critical 591-kb region for bovine carcass weight QTL (CW-2) on chromosome 6 and the Ile-442-Met substitution in NCAPG as a positional candidate. BMC Genet. 10, 43 (2009
44. Quartu M., et al. Neurturin, persephin, and artemin in the human pre- and full-term newborn and adult hippocampus and fascia dentata. Brain Res. 1041, 157-166 (2005
45. Simanainen U., et al. Evidence for increased tissue androgen sensitivity in neurturin knockout mice. J. Endocrinol. 218, 151-163 (2013
46. Oschipok L.W., Teh J., McPhail L.T., & Tetzlaff W. Expression of Semaphorin3C in axotomized rodent facial and rubrospinal neurons. Neurosci. Lett. 434, 113-118 (2008
47. Hernández-Montiel H.L., Tamariz E., Sandoval-Minero M.T., & Varela-Echavarría A. Semaphorins 3A, 3C, and 3F in mesencephalic dopaminergic axon pathfinding. J. Comp. Neurol. 506, 387-397 (2008
48. Gonthier B., et al. Functional interaction between matrix metalloproteinase-3 and semaphorin-3C during cortical axonal growth and guidance. Cereb. Cortex 17, 1712-1721 (2007
49. Ruediger T., et al. Integration of opposing semaphorin guidance cues in cortical axons. Cereb. Cortex 23, 604-614 (2013
50. Niquille M., et al. Transient neuronal populations are required to guide callosal axons: a role for semaphorin 3C. PLoS Biol. 7, e1000230 (2009
51. Pasterkamp R.J., Kolk S.M., Hellemons A.J.C.G.M., & Kolodkin A.L. Expression patterns of semaphorin7A and plexinC1 during rat neural development suggest roles in axon guidance and neuronal migration. BMC Dev. Biol. 7, 98 (2007
52. Brown C.B., et al. PlexinA2 and semaphorin signaling during cardiac neural crest development. Development 128, 3071-3080 (2001
53. Ultanir S.K., et al. Chemical genetic identification of NDR1/2 kinase substrates AAK1 and Rabin8 uncovers their roles in dendrite arborization and spine development. Neuron 73, 1127-1142 (2012
54. Chevallier J., et al. Rab35 regulates neurite outgrowth and cell shape. FEBS Lett. 583, 1096-1101 (2009
55. Ong S.H., et al. FRS2 proteins recruit intracellular signaling pathways by binding to diverse targets on fibroblast growth factor and nerve growth factor receptors. Mol. Cell. Biol. 20, 979-989 (2000
56. Sokol D.K., et al. High levels of Alzheimer β-amyloid precursor protein (APP) in children with severely autistic behavior and aggression. J. Child Neurol. 21, 444-449 (2006
57. Grayton H.M., Missler M., Collier D.A., & Fernandes C. Altered social behaviours in neurexin 1α knockout mice resemble core symptoms in neurodevelopmental disorders. PLoS ONE 8, e67114 (2013
58. Bhoiwala D.L., et al. Overexpression of RCAN1 isoform 4 in mouse neurons leads to a moderate behavioral impairment. Neurol. Res. 35, 79-89 (2013
59. Dierssen M., et al. Behavioral characterization of a mouse model overexpressing DSCR1/RCAN1. PLoS ONE 6, e17010 (2011
60. Kim K.S., Larsen N., Short T., Plastow G., & Rothschild M.F. A missense variant of the porcine melanocortin-4 receptor (MC4R) gene is associated with fatness, growth, and feed intake traits. Mamm. Genome 11, 131-135 (2000
61. Xu P., et al. Double deletion of melanocortin 4 receptors and SAPAP3 corrects compulsive behavior and obesity in mice. Proc. Natl. Acad. Sci. USA 110, 10759-10764 (2013
62. Valette M., et al. Eating behaviour in obese patients with melanocortin-4 receptor mutations: a literature review. Int. J. Obes. (Lond.) 37, 1027-1035 (2013
63. Wojcik S.M., et al. Genetic markers of a Munc13 protein family member, BAIAP3, are gender specifically associated with anxiety and benzodiazepine abuse in mice and humans. Mol. Med. 19, 135-148 (2013
64. Garud N.R., Messer P.W., Buzbas E.O., & Petrov D.A. Recent selective sweeps in North American drosophila melanogaster show signatures of soft sweeps. PLoS Genet. 11, e1005004 (2015
65. Freedman A.H., et al. Genome sequencing highlights the dynamic early history of dogs. PLoS Genet. 10, e1004016 (2014
66. Warmuth V., et al. Reconstructing the origin and spread of horse domestication in the Eurasian steppe. Proc. Natl. Acad. Sci. USA 109, 8202-8206 (2012
67. Turner T.L., Hahn M.W., & Nuzhdin S.V. Genomic islands of speciation in Anopheles gambiae. PLoS Biol. 3, e285 (2005
68. Ludwig A., et al. Twenty-five thousand years of fluctuating selection on leopard complex spotting and congenital night blindness in horses. Phil. Trans. R. Soc. Lond. B 370, 20130386 (2015
69. Vilà C., Seddon J., & Ellegren H. Genes of domestic mammals augmented by backcrossing with wild ancestors. Trends Genet. 21, 214-218 (2005
70. Carneiro M., et al. Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication. Science 345, 1074-1079 (2014
71. Pickrell J.K., & Reich D. Toward a new history and geography of human genes informed by ancient DNA. Trends Genet. 30, 377-389 (2014
72. Larson G., & Burger J. A population genetics view of animal domestication. Trends Genet. 29, 197-205 (2013
73. Girdland Flink L., et al. Establishing the validity of domestication genes using DNA from ancient chickens. Proc. Natl. Acad. Sci. USA 111, 6184-6189 (2014
74. Alexander D.H., Novembre J., & Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664 (2009
75. McKenna A., et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010
76. Frantz L.A.F., et al. Evolution of Tibetan wild boars. Nat. Genet. 47, 188-189 (2015
77. Hudson R.R. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18, 337-338 (2002
78. Thornton K. libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics 19, 2325-2327 (2003
79. Peter B.M., Huerta-Sanchez E., & Nielsen R. Distinguishing between selective sweeps from standing variation and from a de novo mutation. PLoS Genet. 8, e1003011 (2012
80. Wegmann D., Leuenberger C., Neuenschwander S., & Excoffier L. ABCtoolbox: a versatile toolkit for approximate Bayesian computations. BMC Bioinformatics 11, 116 (2010
81. Wegmann D., Leuenberger C., & Excoffier L. Efficient approximate Bayesian computation coupled with Markov chain Monte Carlo without likelihood. Genetics 182, 1207-1218 (2009
82. Leuenberger C., & Wegmann D. Bayesian computation and model selection without likelihoods. Genetics 184, 243-252 (2010
83. Pickrell J.K., & Pritchard J.K. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8, e1002967 (2012
84. Abraham G., & Inouye M. Fast principal component analysis of large-scale genome-wide data. PLoS ONE 9, e93766 (2014
85. Paradis E., Claude J., & Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20, 289-290 (2004
86. Chen G.K., Marjoram P., & Wall J.D. Fast and flexible simulation of DNA sequence data. Genome Res. 19, 136-142 (2009