Signatures of Diversifying Selection in European Pig Breeds

PLoS Genetics

Volumn 9, Issue 4, 2013, Pages

  Wilkinson, Samantha ^a,e   Lu, Zen H ^a   Megens, Hendrik Jan ^b   Archibald, Alan L ^a   Haley, Chris ^a,c   Jackson, Ian J ^a,c   Groenen, Martien A M ^b   Crooijmans, Richard P M A ^b   Ogden, Rob ^d   Wiener, Pamela ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d ROYAL ZOOLOGICAL SOCIETY OF SCOTLAND   (United Kingdom)

^e SCOTTISH AGRICULTURAL COLLEGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BREED DIFFERENCE; CONTROLLED STUDY; DIVERSIFYING SELECTION; DOMESTIC PIG; EAR; EDNRB GENE; EUROPEAN PIG; GENE; GENETIC ASSOCIATION; GENETIC TRAIT; GENOME ANALYSIS; GROWTH; KITLG GENE; LIPID STORAGE; NONHUMAN; OSSIFICATION; PHENOTYPIC VARIATION; PIG FARMING; QUANTITATIVE TRAIT LOCUS; REPRODUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; WILD BOAR; ANIMAL; BREEDING; GENETIC SELECTION; GENETICS; GENOME; GENOMICS; PHENOTYPE; PIG;

SUIDAE; SUS SCROFA;

ANIMALS; BREEDING; GENOME; GENOMICS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SELECTION, GENETIC; SUS SCROFA; SWINE;

EID: 84876877283     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003453     Document Type: Article

References (86)

1. Larson G, Albarella U, Dobney K, Rowley-Conwy P, Schibler J, et al. (2007) Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proceedings of the National Academy of Sciences 104: 15276-15281.
2. Larson G, Dobney K, Albarella U, Fang MY, Matisoo-Smith E, et al. (2005) Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 307: 1618-1621.
3. FAO (2007) The State of the World's Animal Genetic Resources for Food and Agriculture - in brief. Commission on Genetic Resources for Food and Agriculture: FAO, Rome, Italy.
4. Darwin C (1868) The Variation of Animals and Plants under Domestication. London: John Murray.
5. BPA (2002) British Pig Breeds. Trumpington, Cambridge: British Pig Association.
6. Porter V (1993) Pigs. A Handbook to the Breeds of the World. Mountfield, East Sussex: Helm Information, Ltd.
7. Wilkinson S, Haley C, Alderson L, Wiener P, (2011) An empirical assessment of individual-based population genetic statistical techniques: application to British pig breeds. Heredity 106: 261-269.
8. Andersson L, (2001) Genetic dissection of phenotypic diversity in farm animals. Nature Reviews Genetics 2: 130-138.
9. Andersson L, Georges M, (2004) Domestic-animal genomics: deciphering the genetics of complex traits. Nat Rev Genet 5: 202-212.
10. Van Laere A-S, Nguyen M, Braunschweig M, Nezer C, Collette C, et al. (2003) A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig. Nature 425: 832-836.
11. Andersson L, Haley CS, Ellegren H, Knott SA, Johansson M, et al. (1994) Genetic-mapping of quantitative trait loci for growth and fatness in pigs. Science 263: 1771-1774.
12. Knott SA, Marklund L, Haley CS, Andersson K, Davies W, et al. (1998) Multiple marker mapping of quantitative trait loci in a cross between outbred wild boar and large white pigs. Genetics 149: 1069-1080.
13. Buske B, Sternstein I, Brockmann G, (2006) QTL and candidate genes for fecundity in sows. Animal Reproduction Science 95: 167-183.
14. Giuffra E, Evans G, Törnsten A, Wales R, Day A, et al. (1999) The Belt mutation in pigs is an allele at the Dominant white locus. Mammalian Genome 10: 1132-1136.
15. Kijas JMH, Moller M, Plastow G, Andersson L, (2001) A frameshift mutation in MC1R and a high frequency of somatic reversions cause black spotting in pigs. Genetics 158: 779-785.
16. Kijas JMH, Wales R, Törnsten A, Chardon P, Moller M, et al. (1998) Melanocortin receptor 1 (MC1R) mutations and coat color in pigs. Genetics 150: 1177-1185.
17. Wiener P, Wilkinson S, (2011) Deciphering the genetic basis of animal domestication. Proceedings of the Royal Society B: Biological Sciences 278: 3161-3170.
18. Akey JM, Ruhe AL, Akey DT, Wong AK, Connelly CF, et al. (2010) Tracking footprints of artificial selection in the dog genome. Proceedings of the National Academy of Sciences 107: 1160-1165.
19. Boyko AR, Quignon P, Li L, Schoenebeck JJ, Degenhardt JD, et al. (2010) A simple genetic architecture underlies morphological variation in dogs. PLoS Biol 8: e1000451 doi:10.1371/journal.pbio.1000451.
20. Flori L, Fritz S, Jaffrezic F, Boussaha M, Gut I, et al. (2009) The genome response to artificial selection: a case study in dairy cattle. PLoS ONE 4: e6595 doi:10.1371/journal.pone.0006595.
21. Gibbs RA, Taylor JF, Van Tassell CP, Barendse W, Eversoie KA, et al. (2009) Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science 324: 528-532.
22. Kijas JW, Lenstra JA, Hayes B, Boitard S, Porto Neto LR, et al. (2012) Genome-wide analysis of the world's sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biol 10: e1001258 doi:10.1371/journal.pbio.1001258.
23. Qanbari S, Pimentel ECG, Tetens J, Thaller G, Lichtner P, et al. (2010) A genome-wide scan for signatures of recent selection in Holstein cattle. Animal Genetics 41: 377-389.
24. Vaysse A, Ratnakumar A, Derrien T, Axelsson E, Rosengren Pielberg G, et al. (2011) Identification of genomic regions associated with phenotypic variation between dog breeds using selection mapping. PLoS Genet 7: e1002316 doi:10.1371/journal.pgen.1002316.
25. Rubin C-J, Megens H-J, Martinez Barrio A, Maqbool K, Sayyab S, et al. (2012) Strong signatures of selection in the domestic pig genome. Proceedings of the National Academy of Sciences of the United States of America 109: 19529-19536.
26. Sanchez M-P, Iannuccelli N, Basso B, Bidanel J-P, Billon Y, et al. (2007) Identification of QTL with effects on intramuscular fat content and fatty acid composition in a Duroc x Large White cross. BMC Genetics 8: 55.
27. Uemoto Y, Soma Y, Sato S, Ishida M, Shibata T, et al. (2012) Genome-wide mapping for fatty acid composition and melting point of fat in a purebred Duroc pig population. Animal Genetics 43: 27-34.
28. Westerberg R, Mansson JE, Golozoubova V, Shabalina IG, Backlund EC, et al. (2006) ELOVL3 is an important component for early onset of lipid recruitment in brown adipose tissue. Journal of Biological Chemistry 281: 4958-4968.
29. Onteru SK, Fan B, Du ZQ, Garrick DJ, Stalder KJ, et al. (2012) A whole-genome association study for pig reproductive traits. Animal Genetics 43: 18-26.
30. Cieslak M, Reissmann M, Hofreiter M, Ludwig A, (2011) Colours of domestication. Biological Reviews 86: 885-899.
31. Bannasch D, Young A, Myers J, Truve K, Dickinson P, et al. (2010) Localization of canine brachycephaly using an across breed mapping approach. PLoS ONE 5: e9632 doi:10.1371/journal.pone.0009632.
32. Quilez J, Short AD, Martinez V, Kennedy LJ, Ollier W, et al. (2011) A selective sweep of >8 Mb on chromosome 26 in the Boxer genome. BMC Genomics 12: 339.
33. Harlizius B, Rattink AP, de Koning DJ, Faivre M, Joosten RG, et al. (2000) The X Chromosome harbors quantitative trait loci for backfat thickness and intramuscular fat content in pigs. Mammalian Genome 11: 800-802.
34. Groenen MAM, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, et al. (2012) Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491: 393-398.
35. Amaral AJ, Ferretti L, Megens H-J, Crooijmans RPMA, Nie H, et al. (2011) Genome-wide footprints of pig domestication and selection revealed through massive parallel sequencing of pooled DNA. PLoS ONE 6: e14782 doi:10.1371/journal.pone.0014782.
36. Zhang Z, Anthony RV, (1994) Porcine stem-cell factor/c-kit ligand: its molecular-cloning and localization within the uterus. Biology of Reproduction 50: 95-102.
37. Okumura N, Matsumoto T, Hamasima N, Awata T, (2008) Single nucleotide polymorphisms of the KIT and KITLG genes in pigs. Animal Science Journal 79: 303-313.
38. Wei WH, de Koning DJ, Penman JC, Finlayson HA, Archibald AL, et al. (2007) QTL modulating ear size and erectness in pigs. Animal Genetics 38: 222-226.
39. Ren J, Duan Y, Qiao R, Yao F, Zhang Z, et al. (2011) A missense mutation in PPARD causes a major QTL effect on ear size in pigs. PLoS Genet 7: e1002043 doi:10.1371/journal.pgen.1002043.
40. Li P, Xiao S, Wei N, Zhang Z, Huang R, et al. (2012) Fine mapping of a QTL for ear size on porcine chromosome 5 and identification of high mobility group AT-hook 2 (HMGA2) as a positional candidate gene. Genetics Selection Evolution 44: 6.
41. Hellemans J, Preobrazhenska O, Willaert A, Debeer P, Verdonk PCM, et al. (2004) Loss-of-function mutations in LEMD3 result in osteopoikilosis, Buschke-Ollendorff syndrome and melorheostosis. Nat Genet 36: 1213-1218.
42. Barsh GS, (1996) The genetics of pigmentation: From fancy genes to complex traits. Trends in Genetics 12: 299-305.
43. Jackson IJ, (1997) Homologous pigmentation mutations in human, mouse and other model organisms. Human Molecular Genetics 6: 1613-1624.
44. Baxter LL, Hou L, Loftus SK, Pavan WJ, (2004) Spotlight on spotted mice: A review of white spotting mouse mutants and associated human pigmentation disorders. Pigment Cell Research 17: 215-224.
45. Yamada T, Ohtani S, Sakurai T, Tsuji T, Kunieda T, et al. (2006) Reduced expression of the endothelin receptor type B gene in piebald mice caused by insertion of a retroposon-like element in intron 1. Journal of Biological Chemistry 281: 10799-10807.
46. Santschi EM, Purdy AK, Valberg SJ, Vrotsos PD, Kaese H, et al. (1998) Endothelin receptor B polymorphism associated with lethal white foal syndrome in horses. Mammalian Genome 9: 306-309.
47. Fuchs S, Amiel J, Claudel S, Lyonnet S, Corvol P, et al. (2001) Functional characterization of three mutations of the endothelin B receptor gene in patients with Hirschsprung's disease: Evidence for selective loss of G(i) coupling. Molecular Medicine 7: 115-124.
48. Saravanan K, Hariprasad G, Jitesh O, Das U, Dey S, et al. (2007) Endothelin and its receptor interactions: Role of extracellular receptor domain and length of peptide Ligands. Protein and Peptide Letters 14: 779-783.
49. Takasuka T, Sakurai T, Goto K, Furuichi Y, Watanabe T, (1994) Human endothelin receptor ET(B)- amino-acid-sequence requirements for super stable complex-formation with its ligand. Journal of Biological Chemistry 269: 7509-7513.
50. Grantcharova E, Furkert J, Reusch HP, Krell HW, Papsdorf G, et al. (2002) The extracellular N terminus of the endothelin B (ETB) receptor is cleaved by a metalloprotease in an agonist-dependent process. Journal of Biological Chemistry 277: 43933-43941.
51. Verspurten J, Gevaert K, Declercq W, Vandenabeele P, (2009) SitePredicting the cleavage of proteinase substrates. Trends in Biochemical Sciences 34: 319-323.
52. Kaelin CB, Xu X, Hong LZ, David VA, McGowan KA, et al. (2012) Specifying and sustaining pigmentation patterns in domestic and wild cats. Science 337: 1536-1541.
53. Okumura N, Hayashi T, Sekikawa H, Matsumoto T, Mikawa A, et al. (2006) Sequencing, mapping and nucleotide variation of porcine coat colour genes EDNRB, MYO5A, KITLG, SLC45A2, RAB27A, SILV and MITF. Animal Genetics 37: 80-82.
54. Fang M, Larson G, Soares Ribeiro H, Li N, Andersson L, (2009) Contrasting mode of evolution at a coat color locus in wild and domestic pigs. PLoS Genet 5: e1000341 doi:10.1371/journal.pgen.1000341.
55. Li J, Yang H, Li Jr, Li Hp, Ning T, et al. (2010) Artificial selection of the melanocortin receptor 1 gene in Chinese domestic pigs during domestication. Heredity 105: 274-281.
56. Silvers W (1979) The coat colors of mice. New York: Springer Verlag. Online at http://www.informatics.jax.org/wksilvers. Chapter 11.
57. Picardo M, Cardinali G, (2011) The genetic determination of skin pigmentation: KITLG and the KITLG/c-Kit pathway as key players in the onset of human familial pigmentary diseases. Journal of Investigative Dermatology 131: 1182-1185.
58. Wang Z-Q, Si L, Tang Q, Lin D, Fu Z, et al. (2009) Gain-of-function mutation of KIT ligand on melanin synthesis causes familial progressive hyperpigmentation. American Journal of Human Genetics 84: 672-677.
59. Hadjiconstantouras C, Sargent CA, Skinner TM, Archibald AL, Haley CS, et al. (2008) Characterization of the porcine KIT ligand gene: expression analysis, genomic structure, polymorphism detection and association with coat colour traits. Animal Genetics 39: 217-224.
60. Okumura N, Hayashi T, Uenishi H, Fukudome N, Komatsuda A, et al. (2010) Sequence polymorphisms in porcine homologs of murine coat colour-related genes. Animal Genetics 41: 113-121.
61. Miller CT, Beleza S, Pollen AA, Schluter D, Kittles RA, et al. (2007) cis-regulatory changes in kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131: 1179-1189.
62. Sulem P, Gudbjartsson DF, Stacey SN, Helgason A, Rafnar T, et al. (2007) Genetic determinants of hair, eye and skin pigmentation in Europeans. Nature Genetics 39: 1443-1452.
63. Hirooka H, de Koning DJ, Harlizius B, van Arendonk JAM, Rattink AP, et al. (2001) A whole-genome scan for quantitative trait loci affecting teat number in pigs. Journal of Animal Science 79: 2320-2326.
64. Rodriguez C, Tomas A, Alves E, Ramirez O, Arque M, et al. (2005) QTL mapping for teat number in an Iberian-by-Meishan pig intercross. Animal Genetics 36: 490-496.
65. Arnaud-Dabernat S, Bourbon PM, Dierich A, Le Meur M, Daniel JY, (2003) Knockout mice as model systems for studying nm23/NDP kinase gene functions. Application to the nm23-M1 gene. Journal of Bioenergetics and Biomembranes 35: 19-30.
66. Deplagne C, Peuchant E, Moranvillier I, Dubus P, Dabernat S, (2011) The anti-metastatic nm23-1 gene is needed for the final step of mammary duct maturation of the mouse nipple. PLoS ONE 6: e18645 doi:10.1371/journal.pone.0018645.
67. Warriss PD, Kestin SC, Brown SN, Nute GR, (1996) The quality of pork from traditional pig breeds. Meat Focus International 5: 179-182.
68. Cameron ND, Enser MB, (1991) Fatty acid composition of lipid in Longissimus dorsi muscle of Duroc and British Landrace pigs and its relationship with eating quality. Meat Science 29: 295-307.
69. Broberger C, (2005) Brain regulation of food intake and appetite: molecules and networks. Journal of Internal Medicine 258: 301-327.
70. Reynolds CB, Elias AN, Whisnant CS, (2010) Effects of feeding pattern on ghrelin and insulin secretion in pigs. Domestic Animal Endocrinology 39: 90-96.
71. Gondret F, Riquet J, Tacher S, Demars J, Sanchez MP, et al. (2011) Towards candidate genes affecting body fatness at the SSC7 QTL by expression analyses. Journal of Animal Breeding and Genetics 129: 316-324.
72. Epstein H, Bichard M (1984) Pig. In: Mason I, editor. Evolution of Domesticated Animals. London: Longman. pp.145-162.
73. Megens HJ, Crooijmans R, Cristobal MS, Hui X, Li N, et al. (2008) Biodiversity of pig breeds from China and Europe estimated from pooled DNA samples: differences in microsatellite variation between two areas of domestication. Genetics Selection Evolution 40: 103-128.
74. Ramos AM, Crooijmans R, Affara NA, Amaral AJ, Archibald AL, et al. (2009) Design of a high density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology. PLoS ONE 4: e6524 doi:10.1371/journal.pone.0006524.
75. SanCristobal M, Chevalet C, Haley CS, Joosten R, Rattink AP, et al. (2006) Genetic diversity within and between European pig breeds using microsatellite markers. Animal Genetics 37: 189-198.
76. R Core Team (2011) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
77. Wigginton JE, Cutler DJ, Abecasis GR, (2005) A note on exact tests of Hardy-Weinberg equilibrium. American Journal of Human Genetics 76: 887-893.
78. Wright S, (1931) Evolution in Mendelian populations. Genetics 16: 97-159.
79. Wilkinson S, Wiener P, Archibald AL, Law A, Schnabel RD, et al. (2011) Evaluation of approaches for identifying population informative markers from high density SNP Chips. BMC Genetics 12: 45.
80. Weir BS, Cockerham CC, (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
81. Akey JM, Zhang G, Zhang K, Jin L, Shriver MD, (2002) Interrogating a high-density SNP map for signatures of natural selection. Genome Research 12: 1805-1814.
82. Moradi MH, Nejati-Javaremi A, Moradi-Shahrbabak M, Dodds KG, McEwan JC, (2012) Genomic scan of selective sweeps in thin and fat tail sheep breeds for identifying of candidate regions associated with fat deposition. BMC Genetics 13: 10.
83. Badke YM, Bates RO, Ernst CW, Schwab C, Steibel JP, (2012) Estimation of linkage disequilibrium in four US pig breeds. BMC Genomics 13: 24.
84. Falush D, Stephens M, Pritchard JK, (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164: 1567-1587.
85. Zhao K, Wright M, Kimball J, Eizenga G, McClung A, et al. (2010) Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome. PLoS ONE 5: e10780 doi:10.1371/journal.pone.0010780.
86. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.