Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-19T07:55:24.966Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative evaluation of genomic inbreeding parameters in seven commercial and autochthonous pig breeds

Published online by Cambridge University Press:  13 January 2020

G. Schiavo ,
S. Bovo ,
F. Bertolini ,
S. Tinarelli ,
S. Dall’Olio ,
L. Nanni Costa ,
M. Gallo  and
L. Fontanesi Open the ORCID record for L. Fontanesi [Opens in a new window]
G. Schiavo
Affiliation:
Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale G. Fanin 46, 40127Bologna, Italy
S. Bovo
Affiliation:
Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale G. Fanin 46, 40127Bologna, Italy
F. Bertolini
Affiliation:
National Institute of Aquatic Resources, Technical University of Denmark, Kemitorvet, Building 202, 2800Kongens Lyngby, Denmark
S. Tinarelli
Affiliation:
Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale G. Fanin 46, 40127Bologna, Italy Associazione Nazionale Allevatori Suini, Via Nizza 53, 00198Roma, Italy
S. Dall’Olio
Affiliation:
Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale G. Fanin 46, 40127Bologna, Italy
L. Nanni Costa
Affiliation:
Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale G. Fanin 46, 40127Bologna, Italy
M. Gallo
Affiliation:
Associazione Nazionale Allevatori Suini, Via Nizza 53, 00198Roma, Italy
L. Fontanesi*
Affiliation:
Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale G. Fanin 46, 40127Bologna, Italy
*
†E-mail: luca.fontanesi@unibo.it
Get access

Abstract

Single nucleotide polymorphism (SNP) genotyping tools, which can analyse thousands of SNPs covering the whole genome, have opened new opportunities to estimate the inbreeding level of animals directly using genome information. One of the most commonly used genomic inbreeding measures considers the proportion of the autosomal genome covered by runs of homozygosity (ROH), which are defined as continuous and uninterrupted chromosome portions showing homozygosity at all loci. In this study, we analysed the distribution of ROH in three commercial pig breeds (Italian Large White, n = 1968; Italian Duroc, n = 573; and Italian Landrace, n = 46) and four autochthonous breeds (Apulo-Calabrese, n = 90; Casertana, n = 90; Cinta Senese, n = 38; and Nero Siciliano, n = 48) raised in Italy, using SNP data generated from Illumina PorcineSNP60 BeadChip. We calculated ROH-based inbreeding coefficients (FROH) using ROH of different minimum length (1, 2, 4, 8, 16 Mbp) and compared them with several other genomic inbreeding coefficients (including the difference between observed and expected number of homozygous genotypes (FHOM)) and correlated all these genomic-based measures with the pedigree inbreeding coefficient (FPED) calculated for the pigs of some of these breeds. Autochthonous breeds had larger mean size of ROH than all three commercial breeds. FHOM was highly correlated (0.671 to 0.985) with FROH measures in all breeds. Apulo-Calabrese and Casertana had the highest FROH values considering all ROH minimum lengths (ranging from 0.273 to 0.189 and from 0.226 to 0.152, moving from ROH of minimum size of 1 Mbp (FROH1) to 16 Mbp (FROH16)), whereas the lowest FROH values were for Nero Siciliano (from 0.072 to 0.051) and Italian Large White (from 0.117 to 0.042). FROH decreased as the minimum length of ROH increased for all breeds. Italian Duroc had the highest correlations between all FROH measures and FPED (from 0.514 to 0.523) and between FHOM and FPED (0.485). Among all analysed breeds, Cinta Senese had the lowest correlation between FROH and FPED. This might be due to the imperfect measure of FPED, which, mainly in local breeds raised in extensive production systems, cannot consider a higher level of pedigree errors and a potential higher relatedness of the founder population. It appeared that ROH better captured inbreeding information in the analysed breeds and could complement pedigree-based inbreeding coefficients for the management of these genetic resources.

Keywords

autozygositygenetic resourceruns of homozygositysingle nucleotide polymorphismsSus scrofa
Type
Research Article
Information
animal , Volume 14 , Issue 5 , May 2020 , pp. 910 - 920
Copyright
© The Animal Consortium 2020

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

ANAS 2019. Registro Anagrafico. Retrieved on 10 June 2019 from http://www.anas.it/.Google Scholar
Barbato, M, Orozco-terWengel, P, Tapio, M and Bruford, MW 2015. SNeP: a tool to estimate trends in recent effective population size trajectories using genome-wide SNP data. Frontiers in Genetics 6, 109.CrossRefGoogle ScholarPubMed
Bertolini, F, Cardoso, TF, Marras, G, Nicolazzi, EL, Rothschild, MF, Amills, M and AdaptMap consortium 2018a. Genome-wide patterns of homozygosity provide clues about the population history and adaptation of goats. Genetics Selection Evolution 50, 59.CrossRefGoogle ScholarPubMed
Bertolini, F, Schiavo, G, Galimberti, G, Bovo, S, D’Andrea, M, Gallo, M, Buttazzoni, L, Rothschild, MF and Fontanesi, L 2018b. Genome-wide association studies for seven production traits highlight genomic regions useful to dissect dry-cured ham quality and production traits in Duroc heavy pigs. Animal 12, 1777–1784.CrossRefGoogle ScholarPubMed
Bosse, M, Megens, HJ, Madsen, O, Paudel, Y, Frantz, LA, Schook, LB, Crooijmans, RP and Groenen, MA 2012. Regions of homozygosity in the porcine genome: consequence of demography and the recombination landscape. PLoS Genetics 8, e1003100.CrossRefGoogle ScholarPubMed
Ceballos, FC, Joshi, PK, Clark, DW, Ramsay, M and Wilson, JF 2018. Runs of homozygosity: windows into population history and trait architecture. Nature Review Genetics 19, 220–234.CrossRefGoogle ScholarPubMed
Chang, CC, Chow, CC, Tellier, LC, Vattikuti, S, Purcell, SM and Lee, JJ 2015. Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience 4, s13742–015–0047–8.CrossRefGoogle ScholarPubMed
Charlesworth, D and Willis, JH 2009. Fundamental concepts in genetics. The genetics of inbreeding depression. Nature Review Genetics 10, 783–796.CrossRefGoogle Scholar
Ferenčaković, M, Hamzić, E, Gredler, B, Solberg, TR, Klemetsdal, G, Curik, I and Sölkner, J 2013a. Estimates of autozygosity derived from runs of homozygosity: empirical evidence from selected cattle populations. Journal of Animal Breeding and Genetics 130, 286–293.CrossRefGoogle ScholarPubMed
Ferenčaković, M, Solkner, J and Curik, I 2013b. Estimating autozygosity from high throughput information: effects of SNP density and genotyping errors. Genetics Selection Evolution 45, 42.CrossRefGoogle ScholarPubMed
Fernández, A, Rodrigáñez, J, Toro, MA, Rodríguez, MC and Silió, L 2002. Inbreeding effects on the parameters of the growth function in three strains of Iberian pigs. Journal of Animal Science 80, 2267–2275.Google ScholarPubMed
Fisher, RA 1954. A fuller theory of junctions in inbreeding. Heredity 8, 187–197.CrossRefGoogle Scholar
Gibson, J, Morton, NE and Collins, A 2006. Extended tracts of homozygosity in outbred human populations. Human Molecular Genetics 15, 789–795.CrossRefGoogle ScholarPubMed
Gomez-Raya, L, Rodríguez, C, Barragán, C and Silió, L 2015. Genomic inbreeding coefficients based on the distribution of the length of runs of homozygosity in a closed line of Iberian pigs. Genetics Selection Evolution 47, 81.CrossRefGoogle Scholar
Joaquim, LB, Chud, TCS, Marchesi, JAP, Savegnago, RP, Buzanskas, ME, Zanella, R, Cantão, ME, Peixoto, JO, Ledur, MC, Irgang, R and Munari, DP 2019. Genomic structure of a crossbred Landrace pig population. PLoS ONE 14, e0212266.CrossRefGoogle ScholarPubMed
Keller, MC, Visscher, PM and Goddard, ME 2011. Quantification of inbreeding due to distant ancestors and its detection using dense single nucleotide polymorphism data. Genetics 89, 237–249.CrossRefGoogle Scholar
Kirin, M, McQuillan, R, Franklin, CS, Campbell, H, McKeigue, PM and Wilson, JF 2010. Genomic runs of homozygosity record population history and consanguinity. PLoS ONE 5, e13996.CrossRefGoogle ScholarPubMed
Marras, G, Gaspa, G, Sorbolini, S, Dimauro, C, Ajmone-Marsan, P, Valentini, A, Williams, JL and Macciotta, NP 2015. Analysis of runs of homozygosity and their relationship with inbreeding in five cattle breeds farmed in Italy. Animal Genetics 46, 110–121.CrossRefGoogle ScholarPubMed
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. 2016. Animal 10, 746–754.CrossRefGoogle Scholar
McQuillan, R, Leutenegger, A-L, 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. American Journal of Human Genetics 83, 359–372.CrossRefGoogle ScholarPubMed
Muñoz, M, Bozzi, R, García, F, Núñez, Y, Geraci, C, Crovetti, A, García-Casco, J, Alves, E, Škrlep, M, Charneca, R, Martins, JM, Quintanilla, R, Tibau, J, Kušec, G, Djurkin-Kušec, I, Mercat, MJ, Riquet, J, Estellé, J, Zimmer, C, Razmaite, V, Araujo, JP, Radović, Č, Savić, R, Karolyi, D, Gallo, M, Čandek-Potokar, M, Fontanesi, L, Fernández, AI and Óvilo, C 2018. Diversity across major and candidate genes in European local pig breeds. PLoS ONE 13, e0207475.CrossRefGoogle ScholarPubMed
Peripolli, E, Metzger, J, de Lemos, MVA, Stafuzza, NB, Kluska, S, Olivieri, BF, Feitosa, FLB, Berton, MP, Lopes, FB, Munari, DP, Lôbo, RB, Magnabosco, CU, Di Croce, F, Osterstock, J, Denise, S, Pereira, ASC and Baldi, F 2018. Autozygosity islands and ROH patterns in Nellore lineages: evidence of selection for functionally important traits. BMC Genomics 19, 680.CrossRefGoogle ScholarPubMed
Peripolli, E, Munari, DP, Silva, MVGB, Lima, ALF, Irgang, R and Baldi, F 2017. Runs of homozygosity: current knowledge and applications in livestock. Animal Genetics 48, 255–271.CrossRefGoogle ScholarPubMed
Purfield, DC, Berry, DP, McParland, S and Bradley, DG 2012. Runs of homozygosity and population history in cattle. BMC Genetics 13, 70.CrossRefGoogle ScholarPubMed
Purfield, DC, McParland, S, Wall, E and Berry, DP 2017. The distribution of runs of homozygosity and selection signatures in six commercial meat sheep breeds. PLoS ONE 12, e0176780.CrossRefGoogle ScholarPubMed
Russo, V, Fontanesi, L, Dolezal, M, Lipkin, E, Scotti, E, Zambonelli, P, Dall’Olio, S, Bigi, D, Davoli, R, Canavesi, F, Medugorac, I, Föster, M, Sölkner, J, Schiavini, F, Bagnato, A and Soller, M 2012. A whole genome scan for QTL affecting milk protein percentage in Italian Holstein cattle, applying selective milk DNA pooling and multiple marker mapping in a daughter design. Animal Genetics 43 (Suppl. 1), 72–86.CrossRefGoogle Scholar
Saura, M, Fernández, A, Varona, L, Fernández, AI, De Cara, MÁR, Barragán, C and Villanueva, B 2015. Detecting inbreeding depression for reproductive traits in Iberian pigs using genome-wide data. Genetics Selection Evolution 47, 1.CrossRefGoogle ScholarPubMed
Schiavo, G, Bovo, S, Dall’Olio, S, Nanni Costa, L, Tinarelli, S, Gallo, M, Bertolini, F and Fontanesi, L 2019. Comparative evaluation of genomic inbreeding parameters in Italian pig breeds. Italian Journal of Animal Science 18 (Suppl. 1), 118–119.Google Scholar
Schiavo, G, Galimberti, G, Calò, DG, Samorè, AB, Bertolini, F, Russo, V, Gallo, M, Buttazzoni, L and Fontanesi, L 2016. Twenty years of artificial directional selection have shaped the genome of the Italian Large White pig breed. Animal Genetics 47, 181–191.CrossRefGoogle ScholarPubMed
Silió, L, Rodríguez, MC, Fernández, A, Barragán, C, Benítez, R, Óvilo, C and Fernández, AI 2013. Measuring inbreeding and inbreeding depression on pig growth from pedigree or SNP-derived metrics. Journal of Animal Breeding and Genetics 130, 349–360.Google ScholarPubMed
Slate, J, David, P, Dodds, KG, Veenvliet, BA, Glass, BC, Broad, TE and McEwan, JC 2004. Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93, 255.CrossRefGoogle ScholarPubMed
VanRaden, PM, Olson, KM, Wiggans, GR, Cole, JB and Tooker, ME 2011. Genomic inbreeding and relationships among Holsteins, Jerseys, and Brown Swiss. Journal of Dairy Science 94, 5673–5682.CrossRefGoogle ScholarPubMed
Wright, S 1922. Coefficients of inbreeding and relationship. American Naturalist 56, 330–338.CrossRefGoogle Scholar
Yang, B, Cui, L, Perez-Enciso, M, Traspov, A, Crooijmans, RPMA, Zinovieva, N, Schook, LB, Archibald, A, Gatphayak, K, Knorr, C, Triantafyllidis, A, Alexandri, P, Semiadi, G, Hanotte, O, Dias, D, Dovč, P, Uimari, P, Iacolina, L, Scandura, M, Groenen, MAM, Huang, L and Megens, HJ 2017. Genome-wide SNP data unveils the globalization of domesticated pigs. Genetics Selection Evolution 49, 71.CrossRefGoogle ScholarPubMed
Yang, J, Lee, SH, Goddard, ME and Visscher, PM 2011. GCTA: a tool for Genome-wide Complex Trait Analysis. American Journal of Human Genetics 88, 76–82.CrossRefGoogle ScholarPubMed
Zanella, R, Peixoto, JO, Cardoso, FF, Cardoso, LL, Biegelmeyer, P, Cantão, ME, Otaviano, A, Freitas, MS, Caetano, AR and Ledur, MC 2016. Genetic diversity analysis two commercial breeds of pigs using genomic and pedigree data. Genetics Selection Evolution 48, 24.CrossRefGoogle ScholarPubMed
Supplementary material: File

Schiavo et al. supplementary material

Tables S1-S7 and Figure S1

Download Schiavo et al. supplementary material(File)
File 132.9 KB