Origin and Genetic Diversity of Pig Breeds

Abstract

Genetic and archaeological findings suggest that pig domestication began about 9000–10 000 YBP at multiple sites across Eurasia, followed by their subsequent spread at a worldwide scale. Development of local types throughout the centuries led to the foundation, mostly during the nineteenth century, of current modern breeds with defined phenotypes and production abilities. Extensive intercrossing markedly increased the gene pool of these founder populations. For instance, it is well known that many European pig breeds carry Far Eastern haplotypes at high frequencies because of an ancient introgression with Chinese swine. Since then, artificial selection, genetic bottlenecks and inbreeding have significantly modified the allelic diversity of pig breeds. In the next future, state‐of‐the‐art scientific advances as well as conservation programmes will be fundamental to preserve the genetic reservoir of pig breeds as well as to exploit it in the context of artificial selection schemes.

Key Concepts:

  • Pigs were domesticated at multiple locations across Eurasia.

  • Exploratory and commercial journeys favoured the dissemination of European and Far Eastern pigs into Africa and America.

  • England, United States and China were the main centres of breed development during the eighteenth to nineteenth centuries.

  • Genetic variation of pigs has been shaped by the complex interplay of artificial selection, population admixture, inbreeding and genetic drift.

  • Artificial selection is evolution but an accelerated pace; therefore, by comparing breeds that have undergone distinct selective pressures we can glimpse the molecular basis of adaptation.

  • Approximately 20% of local pig breeds face extinction because of dramatic decreases in their census or extensive intercrossing with foreign populations.

  • New genotyping and sequencing technologies will revolutionise knowledge on patterns of diversity in livestock species, including pigs.

Keywords: pig breeds; genetic diversity; wild boar; artificial selection

Figure 1.

Median joining network of 440 mitochondrial D‐loop sequences corresponding to worldwide pig and wild boar (WB) populations. It can be seen that Far Eastern Sus scrofa display higher levels of genetic diversity than their European counterpaarts (most European haplotypes are grouped in a single cluster). It is also worth to highlight that European and Near Eastern mitochondrial haplotypes in general do not cluster together suggesting that both populations have distinct origins.

Figure 2.

Genetic dissection of the relationships between several Sus scrofa population based on the structure analysis of microsatellite data. It can be observed that there are three major groups with European (red), Far Eastern (blue) and mixed (green) ancestry. EWB, European wild boar; AWB, Far Eastern wild boar; AFWB, African wild boar; NEWB, Near Eastern wild boar; SCAP, South and Central American local pigs; MEDLP, Mediterranean and Slav local pigs; ANGLP, Anglo‐Saxon local pigs; INTP, International pig breeds; AFLP, African local pigs and AP, Far Eastern local pigs. Reproduced from Ramírez et al. with permission from Oxford University Press.

Figure 3.

Three Y‐chromosome haplotypes have been identified in Sus scrofa so far, being distributed in two major lineages (HY1+HY2 and HY3) that diverged around 1.27 Mya. In this picture, Y‐chromosome haplotype frequencies at diverse Sus scrofa populations are shown. Abbreviations are indicated in the legend of Figure , with the exception of WAFP (West African pigs) and EAFP (East African pigs). Noteworthy, in these two latter populations differences in haplotype frequencies are dramatic, suggesting that EAFP pigs were strongly introgressed with Far Eastern blood at the paternal level while WAFP did not.

Figure 4.

Frequencies of European (in red) and Far Eastern (in blue) mitochondrial cytochrome b haplotypes in diverse Sus scrofa populations (abbreviations as indicated in the legends of Figure and Figure ). It is worth to highlight the strong Far Eastern genetic signature in Anglosaxon, International and East African pig breeds.

Figure 5.

Haplotype structure around an intron 3 mutation at the insulin‐like growth factor 2 gene with causal effects on muscle growth and leanness. This plot shows the squared correlation (r2) between pairs of loci (colour intensity augments proportionally to r2 values). Haplotype blocks are underlined and the arrow points at the causative intron 3 mutation. Five haplotype blocks were detected, spanning 1, 2, 9, 4 and 0.8 kb respectively. The third block was the largest and contained the causative mutation. From Ojeda et al. with permission from the Genetics Society of America.

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References

Alves E, Ovilo C, Rodríguez MC and Silió L (2003) Mitochondrial DNA sequence variation and phylogenetic relationships among Iberian pigs and other domestic and wild pig populations. Animal Genetics 34(5): 319–324.

Amaral AJ, Megens HJ, Crooijmans RP, Heuven HC and Groenen MA (2008) Linkage disequilibrium decay and haplotype block structure in the pig. Genetics 179(1): 569–579.

Amaral A, Ferretti L, Megens HJ et al. (2009b) Finding Selection Footprints in the Swine Genome Using Massive Parallel Sequencing. Proceedings of the Conference on Next Generation Sequencing: Challenges and Opportunities, Barcelona, Spain.

Amaral A, Megens HJ, Kerstens H et al. (2009a) Application of massive parallel sequencing to whole genome SNP discovery in the porcine genome. BMC Genomics 10: 374.

Bamshad M and Wooding SP (2003) Signatures of natural selection in the human genome. Nature Reviews in Genetics 4(2): 99–111.

Baxter S (1984) Of pigs and men. In: Intensive Pig Production: Environmental Management and Design. London: Granada Publishing Ltd.

Blench RM (2000) A history of pigs in Africa. In: Blench RM and Mac Donald K (eds) Origins and Development of African Livestock: Archaeology, Genetics, Linguistics and Ethnography. Abingdon: Routledge Books.

Boitard S, Chevalet C, Mercat MJ et al. (2010) Genetic variability, structure and assignment of Spanish and French pig populations based on a large sampling. Animal Genetics (in press).

Clop A, Amills M, Noguera JL et al. (2004) Estimating the frequency of Asian cytochrome b haplotypes in standard European and local Spanish pig breeds. Genetics Selection and Evolution 36(1): 97–104.

Dobney K and Larson G (2006) DNA and animal domestication: more windows on an elusive process. Journal of Zoology 269(2): 261–271.

Fabuel E, Barragán C, Silió L, Rodríguez MC and Toro MA (2004) Analysis of genetic diversity and conservation priorities in Iberian pigs based on microsatellite markers. Heredity 93(1): 104–113.

Fang M and Andersson L (2006) Mitochondrial diversity in European and Chinese pigs is consistent with population expansions that occurred prior to domestication. Proceedings of the Royal Society of London. Series B, Biological Sciences 273(1595): 1803–1810.

Giuffra E, Kijas JM, Amarger V et al. (2000) The origin of the domestic pig: independent domestication and subsequent introgression. Genetics 154(4): 1785–1791.

Hammond K and Leitch HW (1998) Genetic resources and the global programme for their management. In: Rothschild MF and Ruvinsky A (eds) The Genetics of the Pig. Wallingford: CABI Publishing.

Hein J, Schierup MK and Wiuf C (2005) Gene Genealogies, Variation and Evolution. New York: Oxford University Press.

Jones GF (1998) Genetic aspects of domestication, common breeds and their origin. In: Rothschild MF and Ruvinsky A (eds) The Genetics of the Pig. Wallingford: CABI Publishing.

Kim SO (1994) Burials, pigs, and political prestige in Neolithic China. Current Anthropology 35(2): 119–141.

Kim TH, Kim KS, Choi BH et al. (2005) Genetic structure of pig breeds from Korea and China using microsatellite loci analysis. Journal of Animal Science 83(10): 2255–2263.

Larson G, Albarella U, Dobney K et al. (2007) Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proceedings of the National Academy of Sciences of the USA 104(39): 15276–15281.

Larson G, Dobney K, Albarella U et al. (2005) Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 307(5715): 1618–1621.

Larson G, Liu R, Zhao X et al. (2010) Patterns of East Asian pig domestication, migration, and turnover revealed by modern and ancient DNA. Proceedings of the National Academy of Sciences of the USA 107(17): 7686–7691.

Levathes LE (1994) When China Ruled the Seas: The Treasure Fleet of the Dragon Throne, 1405–1433. New York: Oxford University Press.

Li SJ, Yang SL, Zhao SH et al. (2004) Genetic diversity analyses of 10 indigenous Chinese pig populations based on 20 microsatellites. Journal of Animal Science 82(2): 368–374.

Luetkemeier ES, Sodhi M, Schook LB and Malhi RS (2010) Multiple Asian pig origins revealed through genomic analyses. Molecular Phylogenetics and Evolution 54(3): 680–686.

Medvedev P, Stanciu M and Brudno M (2009) Computational methods for discovering structural variation with next‐generation sequencing. Nature Methods 6(11 suppl.): S13–S20.

Megens HJ, Crooijmans RP, San Cristobal M 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 and Evolution 40(1): 103–128.

Metzker ML (2010) Sequencing technologies – the next generation. Nature Reviews in Genetics 11(1): 31–46.

Nielsen R, Hellmann I, Hubisz M, Bustamante C and Clark AG (2007) Recent and ongoing selection in the human genome. Nature Reviews in Genetics 8(11): 857–868.

Ojeda A, Huang LS, Ren J et al. (2008) Selection in the making: a worldwide survey of haplotypic diversity around a causative mutation in porcine IGF2. Genetics 178(3): 1639–1652.

Ojeda A, Ramos‐Onsins SE, Marletta D et al. (2010) Evolutionary study of a potential selection target region in the pig. Heredity (in press).

Ojeda A, Rozas J, Folch JM and Perez‐Enciso M (2006) Unexpected high polymorphism at the FABP4 gene unveils a complex history for pig populations. Genetics 174(4): 2119–2127.

Orr DE and Shen YS (2006) World Pig Production, Opportunity or Threat? Proceedings of the 2006 Midwest Swine Nutrition Conference, Indianapolis, Indiana, USA.

Porter V (1993) Pigs: A Handbook to the Breeds of the World. Mountfield: Helm Information Ltd.

Ramírez O, Ojeda A, Tomàs A et al. (2009) Integrating Y‐chromosome, mitochondrial and autosomal data to analyze the origin of pig breeds. Molecular Biology and Evolution 26(9): 2061–2072.

Ramos AM, Crooijmans RP, Affara NA 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(8): e6524.

Rodero A, Delgado JV and Rodero E (1992) Primitive Andalusian livestock and their implications in the discovery of America. Archivos de Zootecnia 41(154): 383–400.

Rubin CJ, Zody MC, Eriksson J et al. (2010) Whole‐genome resequencing reveals loci under selection during chicken domestication. Nature 464(7288): 587–591.

SanCristobal M, Chevalet C, Haley CS et al. (2006) Genetic diversity within and between European pig breeds using microsatellite markers. Animal Genetics 37(3): 189–198.

Scandura M, Iacolina L, Crestanello B et al. (2008) Ancient vs. recent processes as factors shaping the genetic variation of the European wild boar: are the effects of the last glaciation still detectable? Molecular Ecology 17(7): 1745–1762.

Souza CA, Paiva SR, Pereira RW et al. (2009) Iberian origin of Brazilian local pig breeds based on Cytochrome b (MT‐CYB) sequence. Animal Genetics 40(5): 759–762.

Souza CA, Ramayo Y, Megens HJ et al. (2010) Porcine Colonization of the Americas: a 60k SNP Story. Proceedings of the World Conference of Genetics Applied to Livestock Production, Leipzig, Germany.

Taverner MR and Dunkin AC (eds) (1996) Introduction to pig production. Pig Production. The Netherlands: Elsevier Science.

Van Laere AS, Nguyen M, Braunschweig M et al. (2003) A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig. Nature 425(6960): 832–836.

Vidal O, Noguera JL, Amills M et al. (2005) Identification of carcass and meat quality quantitative trait loci in a Landrace pig population selected for growth and leanness. Journal of Animal Science 83(2): 293–300.

Welsh CS, Stewart TS, Schwab C and Blackburn HD (2010) Pedigree analysis of 5 swine breeds in the United States and the implications for genetic conservation. Journal of Animal Science 88(5): 1610–1618.

Wu GS, Yao YG, Qu KX et al. (2007) Population phylogenomic analysis of mitochondrial DNA in wild boars and domestic pigs revealed multiple domestication events in East Asia. Genome Biology 8(11): R245.

Yang SL, Wang ZG, Liu B et al. (2003) Genetic variation and relationships of eighteen Chinese indigenous pig breeds. Genetics Selection and Evolution 35(6): 657–671.

Yuan J, Jianlin H and Blench R (2008) Livestock in ancient China: an archaeozoological perspective. In: Sanchez‐Mazas A, Blench RM and Ross M (eds) Human Migrations in Continental East Asia and Taiwan. Genetic, Linguistic and Archaeological Evidence. Abingdon: Routledge.

Zadik BJ (2005) The Iberian Pig in Spain and the Americas at the Time of Columbus. Master Thesis, University of California, Berkeley, pp. 36–51.

Zeder MA, Emshwiller E, Smith BD and Bradley DG (2006) Documenting domestication: the intersection of genetics and archaeology. Trends in Genetics 22(3): 139–155.

Further Reading

Bruford MW, Bradley DG and Luikart G (2003) DNA markers reveal the complexity of livestock domestication. Nature Reviews in Genetics 4(11): 900–910.

Clutton‐Brock J (1999) A Natural History of Domesticated Mammals. Cambridge: Cambridge University Press.

Du FX, Clutter AC and Lohuis MM (2007) Characterizing linkage disequilibrium in pig populations. International Journal of Biological Sciences 3(3): 166–178.

Manlius N and Gautier A (1999) The wild boar in Egypt. Comptes Rendus de l'Académie des Sciences – Series III – Sciences de la Vie 322(7): 573–577.

Yuan J and Flad RK (2002) Pig domestication in ancient China. Antiquity 76(293): 724–732.

Zeder MA (2006) Documenting Domestication: New Genetic and Archaeological Paradigms. Berkeley: University of California Press.

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Amills, Marcel, Clop, Alex, Ramírez, Oscar, and Pérez‐Enciso, Miguel(Sep 2010) Origin and Genetic Diversity of Pig Breeds. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022884]