BMC Genetics | |
Conservation genomic analysis of domestic and wild pig populations from the Iberian Peninsula | |
Richard PMA Crooijmans1  Miguel Pérez-Enciso3  Mirte Bosse1  Guillermo Ramis2  Martien AM Groenen1  Hendrik-Jan Megens1  Juan Manuel Herrero-Medrano1  | |
[1] Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD Wageningen, The Netherlands;Departamento de Producción Animal, Fac. de Veterinaria, Área de Genética, C.P.30100 Murcia, Spain;Institut Català de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Spain | |
关键词: Iberian Peninsula; Pig; Effective population size; Genetic diversity; SNP; Population genetics; Local breeds; | |
Others : 1086399 DOI : 10.1186/1471-2156-14-106 |
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received in 2013-01-30, accepted in 2013-10-24, 发布年份 2013 | |
【 摘 要 】
Background
Inbreeding is among the major concerns in management of local livestock populations. The effective population size of these populations tends to be small, which enhances the risk of fitness reduction and extinction. High-density SNP data make it possible to undertake novel approaches in conservation genetics of endangered breeds and wild populations.
A total of 97 representative samples of domestic and wild pig populations from the Iberian Peninsula, subjected to different levels of threat with extinction, were genotyped with a 60 K SNP panel. Data analyses based on: (i) allele frequency differences; (ii) linkage disequilibrium and (iii) runs of homozygosity were integrated to study population relationships, inbreeding and demographic history.
Results
The domestic pigs analyzed belonged to local Spanish and Portuguese breeds: Iberian ─ including the variants Retinto Iberian, Negro Iberian and Manchado de Jabugo ─, Bisaro and Chato Murciano. The population structure and persistence of phase analysis suggested high genetic relations between Iberian variants, with recent crossbreeding of Manchado de Jabugo with other pig populations. Chato Murciano showed a high frequency of long runs of homozygosity indicating recent inbreeding and reflecting the recent bottleneck reported by historical records. The Chato Murciano and the Manchado de Jabugo breeds presented the lowest effective population sizes in accordance with their status of highly inbred breeds. The Iberian wild boar presented a high frequency of short runs of homozygosity indicating past small population size but no signs of recent inbreeding. The Iberian breed showed higher genetic similarities with Iberian wild boar than the other domestic breeds.
Conclusions
High-density SNP data provided a consistent overview of population structure, demographic history and inbreeding of minority breeds and wild pig populations from the Iberian Peninsula. Despite the very different background of the populations used, we found a good agreement between the different analyses. Our results are also in agreement with historical reports and provide insight in the events that shaped the current genetic variation of pig populations from the Iberian Peninsula. The results exposed will aid to design and implement strategies for the future management of endangered minority pig breeds and wild populations.
【 授权许可】
2013 Herrero-Medrano et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Muir WM, Wong GK-S, Zhang Y, Wang J, Groenen MAM, Crooijmans RPMA, Megens H-J, Zhang H, Okimoto R, Vereijken A, Jungerius A, Albers GAA, Lawley CT, Delany ME, MacEachern S, Cheng HH: Genome-wide assessment of worldwide chicken SNP genetic diversity indicates significant absence of rare alleles in commercial breeds. Proc Natl Acad Sci USA 2008, 105:17312-17317.
- [2]FAO: Building on gender agrobiodiversity and local knowledge. Food Agr Organ Unit Nation 2006, 1:1-5.
- [3]Barja I: Prey and prey-age preference by the iberian wolf canis lupus signatus in a multiple-prey ecosystem. Wildl Biol 2009, 15:147-154.
- [4]Beltrán-Beck B, Ballesteros C, Vicente J, De la Fuente J, Gortázar C: Progress in oral vaccination against tuberculosis in its main wildlife reservoir in Iberia, the Eurasian wild boar. Vet Med Int 2012, 2012:978501.
- [5]Megens HH-J, Crooijmans RPMA, San Cristobal M, Hui X, Li N, Groenen MAM, Magali SC, Xiao H, Ning L, Martien AMG: Biodiversity of pig breeds from China and Europe estimated from pooled DNA samples: differences in microsatellite variation between two areas of domestication. Genet Sel Evol 2008, 40:103-128.
- [6]Sáez-Royuela , Telleria JL: The increased population of the wild boar (Sus scrofa L.) in Europe. Mamm Rev 1986, 16:97-101.
- [7]Alves E, Fernández AI, Barragán C, Ovilo C, Rodríguez C, Silió L: Inference of hidden population substructure of the Iberian pig breed using multilocus microsatellite data. Spanish J Agr Res 2006, 4:37-46.
- [8]García Dory M, Martínez S, Orozco F: Guía de campo de las razas autóctonas españolas. Madrid: Alianza Editorial; 1990.
- [9]Ramos AM, Crooijmans RPMA, Affara NA, Amaral AJ, Archibald AL, Beever JE, Bendixen C, Churcher C, Clark R, Dehais P, Hansen MS, Hedegaard J, Hu ZL, Kerstens HH, Law AS, Megens H-J, Milan D, Nonneman DJ, Rohrer GA, Rothschild MF, Smith TPL, Schnabel RD, Van Tassell CP, Taylor JF, Wiedmann RT, Schook LB, Groenen MAM: Design of a high density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology. PloS One 2009, 4:e6524.
- [10]Duijvesteijn N, Knol EF, Merks JWM, Crooijmans RPMA, Groenen MAM, Bovenhuis H, Harlizius B: A genome-wide association study on androstenone levels in pigs reveals a cluster of candidate genes on chromosome 6. BMC Genet 2010, 11:42.
- [11]Ponsuksili S, Murani E, Brand B, Schwerin M, Wimmers K: Integrating expression profiling and whole-genome association for dissection of fat traits in a porcine model. J Lipid Res 2011, 52:668-678.
- [12]Goedbloed DJ, Megens HJ, Van Hooft P, Herrero-Medrano JM, Lutz W, Alexandri P, Crooijmans RPMA, Groenen MAM, Van Wieren SE, Ydenberg RC, Prins HHT: Genome-wide single nucleotide polymorphism analysis reveals recent genetic introgression from domestic pigs into Northwest European wild boar populations. Mol Ecol 2012, 22:856-866.
- [13]Bosse M, Megens H-J, Madsen O, Paudel Y, Frantz LAF, Schook LB, Crooijmans RPMA, Groenen MAM: Regions of homozygosity in the porcine genome: consequence of demography and the recombination landscape. PLoS Genet 2012, 8:e1003100.
- [14]Hayes BJ, Visscher PM, McPartlan HC, Goddard ME: Novel multilocus measure of linkage disequilibrium to estimate past effective population size. Genome Res 2003, 13:635-643.
- [15]PW DRa, Hayes BJ, Spelman RJ, Goddard ME: Linkage disequilibrium and persistence of phase in Holstein-Friesian, Jersey and Angus cattle. Genetics 2008, 179:1503-1512.
- [16]Purfield DC, Berry DP, McParland S, Bradley DG: Runs of homozygosity and population history in cattle. BMC Genet 2012, 13:70.
- [17]Amaral AJ, Ferretti L, Megens H-J, Crooijmans RPMA, Nie H, Ramos-Onsins SE, Perez-Enciso M, Schook LB, Groenen MAM: Genome-wide footprints of pig domestication and selection revealed through massive parallel sequencing of pooled DNA. PloS One 2011, 6:e14782.
- [18]Rubin C-J, Megens H-J, Barrio AM, Maqbool K, Sayyab S, Schwochow D, Wang C, Carlborg O, Jern P, Jorgensen CB, Archibald AL, Fredholm M, Groenen MAM, Andersson L: Strong signatures of selection in the domestic pig genome. Proc Natl Acad Sci USA 2012, 109:19529-19536.
- [19]Amaral AJ, Megens H-J, Crooijmans RPMA, Heuven HCM, Groenen MAM: Linkage disequilibrium decay and haplotype block structure in the pig. Genetics 2008, 179:569-579.
- [20]Tortereau F, Servin B, Frantz L, Megens H-J, Milan D, Rohrer G, Wiedmann R, Beever J, Archibald AL, Schook LB, Groenen MAM: A high density recombination map of the pig reveals a correlation between sex-specific recombination and GC content. BMC Genom 2012, 13:586. BioMed Central Full Text
- [21]Wilkinson S, Archibald AL, Haley CS, Megens H-J, Crooijmans RPMA, Groenen MAM, Wiener P, Ogden R: Development of a genetic tool for product regulation in the diverse British pig breed market. BMC Genom 2012, 13:580. BioMed Central Full Text
- [22]Ramos AM, Megens HJ, Crooijmans RPMA, Schook LB, Groenen MAM: Identification of high utility SNPs for population assignment and traceability purposes in the pig using high-throughput sequencing. Anim Genet 2011, 42:613-620.
- [23]Herrero-Medrano JM, Megens HJ, Crooijmans RP, Abellaneda JM, Ramis G: Farm-by-farm analysis of microsatellite, mtDNA and SNP genotype data reveals inbreeding and crossbreeding as threats to the survival of a native Spanish pig breed. Anim Genet 2013, 44:259-266.
- [24]Badke YM, Bates RO, Ernst CW, Schwab C, Steibel JP: Estimation of linkage disequilibrium in four US pig breeds. BMC Genom 2012, 13:24. BioMed Central Full Text
- [25]Uimari P, Tapio M: Extent of linkage disequilibrium and effective population size in Finnish Landrace and Finnish Yorkshire pig breeds. J Anim Sci 2011, 89:609-614.
- [26]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 2005, 14:2611-2620.
- [27]Sved JA: Linkage disequilibrium of chromosome segments. Theor Popul Biol 1971, 141:125-141.
- [28]Reich DE, Cargill M, Bolk S, Ireland J, Sabeti PC, Richter DJ, Lavery T, Kouyoumjian R, Farhadian SF, Ward R, Lander ES: Linkage disequilibrium in the human genome. Nature 2001, 411:199-204.
- [29]Megens H-J, Crooijmans RPMA, Bastiaansen JWM, Kerstens HHD, Coster A, Jalving R, Vereijken A, Silva P, Muir WM, Cheng HH, Hanotte O, Groenen MAM: Comparison of linkage disequilibrium and haplotype diversity on macro- and microchromosomes in chicken. BMC Genet 2009, 10:86.
- [30]Ardlie KG, Kruglyak L, Seielstad M: Patterns of linkage disequilibrium in the human genome. Nat Rev Genet 2002, 3:299-309.
- [31]Tenesa A, Navarro P, Hayes BJ, Duffy DL, Clarke GM, Goddard ME, Visscher PM: Recent human effective population size estimated from linkage disequilibrium. Genome Res 2007, 17:520-526.
- [32]Downing T, Imamura H, Decuypere S, Clark TG, Coombs GH, Cotton JA, Hilley JD, De DS, Maes I, Mottram JC, Quail MA, Rijal S, Sanders M, Stark O, Sundar S, Vanaerschot M, Hertz-fowler C, Dujardin J, Berriman M: Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into population structure and mechanisms of drug resistance. Genome Res 2011, 21:2143-2156.
- [33]Gautier M, Laloë D, Moazami-Goudarzi K: Insights into the genetic history of French cattle from dense SNP data on 47 worldwide breeds. PloS One 2010, 5:e13038.
- [34]Decker JE, Pires JC, Conant GC, McKay SD, Heaton MP, Chen K, Cooper A, Vilkki J, Seabury CM, Caetano AR, Johnson GS, Brenneman RA, Hanotte O, Eggert LS, Wiener P, Kim J-J, Kim KS, Sonstegard TS, Van Tassell CP, Neibergs HL, McEwan JC, Brauning R, Coutinho LL, Babar ME, Wilson GA, McClure MC, Rolf MM, Kim J, Schnabel RD, Taylor JF: Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics. Proc Natl Acad Sci USA 2009, 106:18644-18649.
- [35]Berthouly C, Maillard JC, Pham Doan L, Nhu Van T, Bed’Hom B, Leroy G, Hoang Thanh H, Laloë D, Bruneau N, Vu Chi C, Nguyen Dang V, Verrier E, Rognon X: Revealing fine scale subpopulation structure in the Vietnamese H’Mong cattle breed for conservation purposes. BMC Genet 2010, 11:45.
- [36]Druml T, Salajpal K, Dikic M, Urosevic M, Grilz-Seger G, Baumung R: Genetic diversity, population structure and subdivision of local Balkan pig breeds in Austria, Croatia, Serbia and Bosnia-Herzegovina and its practical value in conservation programs. Genet Sel Evol 2012, 44:5. BioMed Central Full Text
- [37]McKay SD, Schnabel RD, Murdoch BM, Matukumalli LK, Aerts J, Coppieters W, Crews D, Dias Neto E, Gill CA, Gao C, Mannen H, Wang Z, Van Tassell CP, Williams JL, Taylor JF, Moore SS: An assessment of population structure in eight breeds of cattle using a whole genome SNP panel. BMC Genet 2008, 9:37.
- [38]Royo LJ, Alvarez I, Fernández I, Pérez-Pardal L, Alvarez-Sevilla A, Godinho R, Ferrand N, Goyache F: Genetic characterisation of Celtic-Iberian pig breeds using microsatellites. In Proceedings of the 6 th International Symposium on the Mediterranean Pig: 11-13 October 2007. Edited by Università di Bologna, Italy. Messina, Italy; 2007:32-35.
- [39]Kirin M, McQuillan R, Franklin CS, Campbell H, McKeigue PM, Wilson JF: Genomic runs of homozygosity record population history and consanguinity. PloS One 2010, 5:e13996.
- [40]Frankham R, Ralls K: Conservation biology: inbreeding leads to extinction. Nature 1998, 392:441-442.
- [41]Wang J: Estimation of effective population sizes from data on genetic markers. Phil Trans Roy Soc Lond B Biol Sci 2005, 360:1395-1409.
- [42]Hill WG: Estimation of effective population size from data on linkage disequilibrium. Genet Res 1981, 38:209-216.
- [43]Park L: Effective population size of current human population. Genet Res 2011, 31:1-10.
- [44]Waples RS, England PR: Estimating contemporary effective population size on the basis of linkage disequilibrium in the face of migration. Genetics 2011, 189:633-644.
- [45]Pemberton TJ, Absher D, Feldman MW, Myers RM, Rosenberg NA, Li JZ: Genomic patterns of homozygosity in worldwide human populations. Am J Hum Genet 2012, 91:275-292.
- [46]Mcquillan R, Leutenegger A, Abdel-rahman R, Franklin CS, Pericic M, Barac-lauc L, Smolej-narancic N, Janicijevic B, Polasek O, Tenesa A, Macleod AK, Farrington SM, Rudan P, Hayward C, Vitart V, Rudan I, Wild SH, Dunlop MG, Wright AF, Campbell H, Wilson JF: Runs of homozygosity in European populations. Am J Hum Genet 2008, 83:359-372.
- [47]Alves PC, Pinheiro I, Godinho R, Vicente J, Gortázar C, Scandura M: Genetic diversity of wild boar populations and domestic pig breeds (Sus scrofa) in South-western Europe. Biol J Linn Soc 2010, 101:797-822.
- [48]Esteve-Codina A, Kofler R, Himmelbauer H, Ferretti L, Vivancos AP, Groenen MAM, Folch JM, Rodríguez MC, Pérez-Enciso M: Partial short-read sequencing of a highly inbred Iberian pig and genomics inference thereof. Heredity 2011, 107:256-264.
- [49]Stumpf MPH, McVean GAT: Estimating recombination rates from population-genetic data. Nat Rev Genet 2003, 4:959-968.
- [50]Apollonio M, Randi E, Toso S: The systematics of the wildboar (Sus scrofa L.) in Italy. Bollettino di Zoologia 1988, 3:213-221.
- [51]Ferreira E, Souto L, Soares AMVM, Fonseca C: Genetic structure of the wild boar population in Portugal: evidence of a recent bottleneck. Mammalian Biology - Zeitschrift für Säugetierkunde 2009, 74:274-285.
- [52]Groenen MAM, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF, Rogel-Gaillard C, Park C, Milan D, Megens H-J, Li S, Larkin DM, Kim H, Frantz LAF, Caccamo M, Ahn H, Aken BL, Anselmo A, Anthon C, Auvil L, Badaoui B, Beattie CW, Bendixen C, Berman D, Blecha F, Blomberg J, Bolund L, Bosse M, Botti S, Bujie Z, Bystrom M, Capitanu B, et al.: Analyses of pig genomes provide insight into porcine demography and evolution. Nature 2012, 491:393-398.
- [53]Ottoni C, Flink LG, Evin A, Geörg C, De Cupere B, Van Neer W, Bartosiewicz L, Linderholm A, Barnett R, Peters J, Decorte R, Waelkens M, Vanderheyden N, Ricaut F-X, Cakirlar C, Cevik O, Hoelzel AR, Mashkour M, Karimlu AFM, Seno SS, Daujat J, Brock F, Pinhasi R, Hongo H, Perez-Enciso M, Rasmussen M, Frantz L, Megens H-J, Crooijmans R, Groenen MAM, et al.: Pig domestication and human-mediated dispersal in western Eurasia revealed through ancient DNA and geometric morphometrics. Mol Biol Evol 2013, 30:824-832.
- [54]Larson G, Burger J: A population genetics view of animal domestication. Trends Genet 2013, 29:197-205.
- [55]Larson G, Albarella U, Dobney K, Rowley-Conwy P, Schibler J, Tresset A, Vigne J-D, Edwards CJ, Schlumbaum A, Dinu A, Balaçsescu A, Dolman G, Tagliacozzo A, Manaseryan N, Miracle P, Van Wijngaarden-Bakker L, Masseti M, Bradley DG, Cooper A: Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proc Natl Acad Sci USA 2007, 104:15276-15281.
- [56]Alves E, Ovilo C, Rodríguez MC, Silió L: Mitochondrial DNA sequence variation and phylogenetic relationships among Iberian pigs and other domestic and wild pig populations. Anim Genet 2003, 34:319-324.
- [57]Van Asch B, Pereira F, Santos LS, Carneiro J, Santos N, Amorim A: Mitochondrial lineages reveal intense gene flow between Iberian wild boars and South Iberian pig breeds. Anim Genet 2012, 43:35-41.
- [58]Nei M: Genetic distance between populations. Am Nat 1972, 106:283-292.
- [59]Liu K, Muse SV: PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 2005, 21:2128-2129.
- [60]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
- [61]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-959.
- [62]Earl DA, vonHoldt BM: Structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conservat Genet Resour 2011, 4:359-361.
- [63]Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D: Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 2006, 38:904-909.
- [64]Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, De Bakker PIW, Daly MJ, Sham PC: PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007, 81:559-575.
- [65]Barrett JC, Fry B, Maller J, Daly MJ: Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005, 21:263-265.