Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-20T09:37:32.952Z Has data issue: false hasContentIssue false
  • English
  • Français

Genome-wide analysis in endangered populations: a case study in Barbaresca sheep

Published online by Cambridge University Press:  12 January 2017

S. Mastrangelo ,
B. Portolano ,
R. Di Gerlando ,
R. Ciampolini ,
M. Tolone ,
M. T. Sardina  and
The International Sheep Genomics Consortium
S. Mastrangelo*
Affiliation:
Dipartimento Scienze Agrarie e Forestali, Università degli Studi di Palermo, 90128 Palermo, Italy
B. Portolano
Affiliation:
Dipartimento Scienze Agrarie e Forestali, Università degli Studi di Palermo, 90128 Palermo, Italy
R. Di Gerlando
Affiliation:
Dipartimento Scienze Agrarie e Forestali, Università degli Studi di Palermo, 90128 Palermo, Italy
R. Ciampolini
Affiliation:
Dipartimento di Scienze Veterinarie, Università degli Studi di Pisa, 56100 Pisa, Italy
M. Tolone
Affiliation:
Dipartimento Scienze Agrarie e Forestali, Università degli Studi di Palermo, 90128 Palermo, Italy
M. T. Sardina
Affiliation:
Dipartimento Scienze Agrarie e Forestali, Università degli Studi di Palermo, 90128 Palermo, Italy
*
†E-mail: [email protected]
Get access

Abstract

Analysis of genomic data is becoming increasingly common in the livestock industry and the findings have been an invaluable resource for effective management of breeding programs in small and endangered populations. In this paper, with the goal of highlighting the potential of genomic analysis for small and endangered populations, genome-wide levels of linkage disequilibrium, measured as the squared correlation coefficient of allele frequencies at a pair of loci, effective population size, runs of homozygosity (ROH) and genetic diversity parameters, were estimated in Barbaresca sheep using Illumina OvineSNP50K array data. Moreover, the breed’s genetic structure and its relationship with other breeds were investigated. Levels of pairwise linkage disequilibrium decreased with increasing distance between single nucleotide polymorphisms. An average correlation coefficient <0.25 was found for markers located up to 50 kb apart. Therefore, these results support the need to use denser single nucleotide polymorphism panels for high power association mapping and genomic selection efficiency in future breeding programs. The estimate of past effective population size ranged from 747 animals 250 generations ago to 28 animals five generations ago, whereas the contemporary effective population size was 25 animals. A total of 637 ROH were identified, most of which were short (67%) and ranged from 1 to 10 Mb. The genetic analyses revealed that the Barbaresca breed tended to display lower variability than other Sicilian breeds. Recent inbreeding was evident, according to the ROH analysis. All the investigated parameters showed a comparatively narrow genetic base and indicated an endangered status for Barbaresca. Multidimensional scaling, model-based clustering, measurement of population differentiation, neighbor networks and haplotype sharing distinguished Barbaresca from other breeds, showed a low level of admixture with the other breeds considered in this study, and indicated clear genetic differences compared with other breeds. Attention should be given to the conservation of Barbaresca due to its critical conservation status. In this context, genomic information may have a crucial role in management of small and endangered populations.

Keywords

OvineSNP50Ksheeppopulation structurelinkage disequilibriumlivestock conservation
Type
Research Article
Information
animal , Volume 11 , Issue 7 , July 2017 , pp. 1107 - 1116
Copyright
© The Animal Consortium 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexander, DH and Lange, K 2011. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics 12, 246.Google Scholar
Al-Mamun, HA, Clark, SA, Kwan, P and Gondro, C 2015. Genome-wide linkage disequilibrium and genetic diversity in five populations of Australian domestic sheep. Genetics Selection Evolution 47, 1–14.Google Scholar
ASSONAPA 2014. Associazione Nazionale della Pastorizia. Available from http://www.assonapa.it/norme_ecc/Consistenze_Caprini.htm.Google Scholar
Barrett, JC, Fry, B, Maller, J and Daly, MJ 2005. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263–265.Google Scholar
Beynon, SE, Slavov, GT, Farré, M, Sunduimijid, B, Waddams, K, Davies, B, Haresign, W, Kijas, J, MacLeod, IM, Newbold, CJ, Davies, L and Larkin, DM 2015. Population structure and history of the Welsh sheep breeds determined by whole genome genotyping. BMC Genetics 16, 65.Google Scholar
Bohmanova, J, Sargolzaei, M and Schenkel, FS 2010. Characteristics of linkage disequilibrium in North American Holsteins. BMC Genomics 11, 421.Google Scholar
Brito, LF, Jafarikia, M, Grossi, DA, Kijas, JW, Porto-Neto, LR, Ventura, RV, Salgorzaei, M and Schenkel, FS 2015. Characterization of linkage disequilibrium, consistency of gametic phase and admixture in Australian and Canadian goats. BMC Genetics 16, 67.Google Scholar
Caballero, A and Toro, MA 2002. Analysis of genetic diversity for the management of conserved subdivided populations. Conservation Genetics 3, 289–299.Google Scholar
Ciani, E, Ciampolini, R, D’Andrea, M, Castellana, E, Cecchi, F, Incoronato, C, D’Angelo, F, Albenzio, M, Pilla, F, Matassino, D and Cianci, D 2013a. Analysis of genetic variability within and among Italian sheep breeds reveals population stratification and suggests the presence of a phylogeographic gradient. Small Ruminant Research 112, 21–27.CrossRefGoogle Scholar
Ciani, E, Crepaldi, P, Nicoloso, L, Lasagna, E, Sarti, FM, Moioli, B, Napolitano, F, Carta, A, Usai, G, D’Andrea, M, Marletta, D, Ciampolini, R, Riggio, V, Occidente, M, Matassino, D, Kompan, D, Modesto, P, Macciotta, N, Ajmone-Marsan, P and Pilla, F 2013b. Genome-wide analysis of Italian sheep diversity reveals a strong geographic pattern and cryptic relationships between breeds. Animal Genetics 45, 256–266.Google Scholar
Ciani, E, Lasagna, E, D’Andrea, M, Alloggio, I, Marroni, F, Ceccobelli, S, Delgado Bermejo, JV, Sarti, FM, Kijas, J, Lenstra, JA and Pilla, F, International Sheep Genomics Consortium 2015. Merino and Merino-derived sheep breeds: a genome-wide intercontinental study. Genetics Selection Evolution 47, 1–12.Google Scholar
Corbin, LJ, Blott, SC, Swinburne, JE, Vaudin, M, Bishop, SC and Woolliams, JA 2010. Linkage disequilibrium and historical effective population size in the Thoroughbred horse. Animal Genetics 41, 8–15.Google Scholar
Corbin, LJ, Liu, AYH, Bishop, SC and Woolliams, JA 2012. Estimation of historical effective population size using linkage disequilibria with marker data. Journal of Animal Breeding and Genetics 129, 257–270.Google Scholar
de Roos, APW, Hayes, BJ, Spelman, RJ and Goddard, ME 2008. Linkage disequilibrium and persistence of phase in Holstein-Friesian, Jersey and Angus Cattle. Genetics 179, 1503–1512.Google Scholar
Do, C, Waples, RS, Peel, D, Macbeth, GM, Tillett, BJ and Ovenden, JR 2014. NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size Ne from genetic data. Molecular Ecology Resources 14, 209–214.Google Scholar
England, PR, Cornuet, JM, Berthier, P, Tallmon, DA and Luikart, G 2006. Estimating effective population size from linkage disequilibrium: severe bias in small samples. Conservation Genetics 2, 303–308.CrossRefGoogle Scholar
Falush, D, van Dorp, L and Lawson, D 2016. A tutorial on how (not) to over-interpret structure/admixture bar plots. bioRxiv, 066431.Google Scholar
Fernández, J, Toro, MA and Caballero, A 2008. Management of subdivided populations in conservation programs: development of a novel dynamic system. Genetics 179, 683–692.Google Scholar
Fernández, J, Meuwissen, THE, Toro, MA and Mäki-Tanila, A 2011. Management of genetic diversity in small farm animal populations. Animal 5, 1684–1698.CrossRefGoogle ScholarPubMed
Frankham, R, Bradshaw, CJA and Brook, BW 2014. Genetics in conservation and management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biological Conservation 170, 56–63.Google Scholar
García-Gámez, E, Sahana, G, Gutiérrez-Gil, B and Arranz, JJ 2012. Linkage disequilibrium and inbreeding estimation in Spanish Churra sheep. BMC Genetics 13, 43.Google Scholar
Gibson, J, Morton, N and Collins, A 2006. Extended tracts of homozygosity in outbred human populations. Human Molecular Genetics 15, 789–795.Google Scholar
Hayes, BJ, Visscher, PM, McPartlan, HC and Goddard, ME 2003. Novel multilocus measure of linkage disequilibrium to estimate past effective population size. Genome Research 13, 635–643.Google Scholar
Hill, WG and Robertson, A 1968. Linkage disequilibrium in finite populations. Theoretical Applied Genetics 38, 226–231.Google Scholar
Huson, DH and Bryant, D 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology Evolution 23, 254–267.CrossRefGoogle ScholarPubMed
Kijas, JW, Lenstra, JA, Hayes, B, Boitard, S, Porto-Neto, LR, Cristobal, MS, Servin, B, McCulloch, R, Whan, V, Gietzen, K, Paiva, S, Barendse, W, Ciani, E, Raadsma, H, McEwan, J and Dalrymple, B, International Sheep Genomics Consortium 2012. Genome-Wide Analysis of the world’s sheep breeds reveals high levels of historic mixture and strong recent selection. PLos Biology 10, e1001258.CrossRefGoogle ScholarPubMed
Kijas, JW, Porto‐Neto, L, Dominik, S, Reverter, A, Bunch, R, McCulloch, R, Hayes, BJ, Brauning, R and McEwan, J, International Sheep Genomics Consortium 2014. Linkage disequilibrium over short physical distances measured in sheep using a high‐density SNP chip. Animal Genetics 45, 754–757.Google Scholar
Lawson, DJ, Hellenthal, G, Myers, S and Falush, D 2012. Inference of population structure using dense haplotype data. PLoS Genetics 8, e1002453.CrossRefGoogle ScholarPubMed
Lencz, T, Lambert, C, De Rosse, P, Burdick, KE, Morgan, TV, Kane, JM, Kucherlapati, R and Malhotra, AK 2007. Runs of homozygosity reveal highly penetrant recessive loci in schizophrenia. Proceedings of the National Academy of Sciences 104, 19942–19947.Google Scholar
Maples, BK, Gravel, S, Kenny, EE and Bustamante, CD 2013. RFMix: a discriminative modeling approach for rapid and robust local-ancestry inference. The American Journal of Human Genetics 93, 278–288.Google Scholar
Mastrangelo, S, Di Gerlando, R, Tolone, M, Tortorici, L, Sardina, MT and Portolano, B, International Sheep Genomics Consortium 2014. Genome wide linkage disequilibrium and genetic structure in sicilian dairy sheep breeds. BMC Genetics 15, 108.Google Scholar
Mastrangelo, S, Tolone, M, Di Gerlando, R, Fontanesi, L, Sardina, MT and Portolano, B 2016. Genomic inbreeding estimation in small populations: evaluation of runs of homozygosity in three local dairy cattle breeds. Animal 10, 746–754.Google Scholar
McQuillan, R, Leutenegger, AL, 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 and Wilson, JF 2008. Runs of homozygosity in European populations. The American Journal of Human Genetics 83, 359–372.Google Scholar
Peter, BM 2016. Admixture, population structure, and F-statistics. Genetics 202, 1485–1501.Google Scholar
Purcell, S, Neale, B, Todd-Brown, K, Thomas, L, Ferreira, MA, Bender, D, Maller, J, Sklar, P, de Bakker, PI, Daly, MJ and Sham, PC 2007. PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics 81, 559–575.Google Scholar
Purfield, DC, Berry, DP, McParland, S and Bradley, DG 2012. Runs of homozygosity and population history in cattle. BMC Genetics 13, 70.Google Scholar
Qanbari, S, Pimentel, EC, Tetens, J, Thaller, G, Lichtner, P, Sharifi, AR and Simianer, H 2010. The pattern of linkage disequilibrium in German Holstein cattle. Animal Genetics 41, 346–356.Google Scholar
R Development Core Team 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Raymond, M and Rousset, F 1995. GENEPOP population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.Google Scholar
Rodríguez-Ramilo, ST, Fernández, J, Toro, MA, Hernández, D and Villanueva, B 2015. Genome-wide estimates of coancestry, inbreeding and effective population size in the Spanish Holstein population. PLoS One 10, 4.Google Scholar
Sved, JA 1971. Linkage disequilibrium of chromosome segments. Theoretical Population Biology 141, 125–141.Google Scholar
Tenesa, A, Navarro, P, Hayes, BJ, Duffy, DL, Clarke, GM, Goddard, ME and Visscher, PM 2007. Recent human effective population size estimated from linkage disequilibrium. Genome Research 17, 520–526.Google Scholar
Tolone, M, Mastrangelo, S, Rosa, AJM and Portolano, B 2012. Genetic diversity and population structure of Sicilian sheep breeds using microsatellite markers. Small Ruminant Research 102, 18–25.Google Scholar
Veroneze, R, Lopes, PS, Guimaraes, SEF, Silva, FF, Lopes, MS, Harlizius, B and Knol, EF 2013. Linkage disequilibrium and haplotype block structure in six commercial pig lines. Journal of Animal Science 91, 3493–3501.Google Scholar
Wang, JL 2005. Estimation of effective population sizes from data on genetic markers. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 1395–1409.CrossRefGoogle ScholarPubMed
Waples, RS and Do, C 2008. LDNE: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources 8, 753–756.Google Scholar
Supplementary material: File

Mastrangelo et al. supplementary material

Tables S1-S4

Download Mastrangelo et al. supplementary material(File)
File 19.5 KB
Supplementary material: File

Mastrangelo et al. supplementary material

Figure S1

Download Mastrangelo et al. supplementary material(File)
File 268.9 KB