Original Article
Analysis of runs of homozygosity and their relationship with inbreeding in five cattle breeds farmed in Italy
Summary
Increased inbreeding is an inevitable consequence of selection in livestock populations. The analysis of high‐density single nucleotide polymorphisms (SNPs) facilitates the identification of long and uninterrupted runs of homozygosity (ROH) that can be used to identify chromosomal regions that are identical by descent. In this work, the distribution of ROH of different lengths in five Italian cattle breeds is described. A total of 4095 bulls from five cattle breeds (2093 Italian Holstein, 749 Italian Brown, 364 Piedmontese, 410 Marchigiana and 479 Italian Simmental) were genotyped at 54K SNP loci. ROH were identified and used to estimate molecular inbreeding coefficients (FROH), which were compared with inbreeding coefficients estimated from pedigree information (FPED) and using the genomic relationship matrix (FGRM). The average number of ROH per animal ranged from 54 ± 7.2 in Piedmontese to 94.6 ± 11.6 in Italian Brown. The highest number of short ROH (related to ancient consanguinity) was found in Piedmontese, followed by Simmental. The Italian Brown and Holstein had a higher proportion of longer ROH distributed across the whole genome, revealing recent inbreeding. The FPED were moderately correlated with FROH > 1 Mb (0.662, 0.700 and 0.669 in Italian Brown, Italian Holstein and Italian Simmental respectively) but poorly correlated with FGRM (0.134, 0.128 and 0.448 for Italian Brown, Italian Holstein and Italian Simmental respectively). The inclusion of ROH > 8 Mb in the inbreeding calculation improved the correlation of FROH with FPED and FGRM. ROH are a direct measure of autozygosity at the DNA level and can overcome approximations and errors resulting from incomplete pedigree data. In populations with high linkage disequilibrium (LD) and recent inbreeding (e.g. Italian Holstein and Italian Brown), a medium‐density marker panel, such as the one used here, may provide a good estimate of inbreeding. However, in populations with low LD and ancient inbreeding, marker density would have to be increased to identify short ROH that are identical by descent more precisely.
Citing Literature
Number of times cited according to CrossRef: 59
- Seyed Mohammad Ghoreishifar, Hossein Moradi-Shahrbabak, Mohammad Hossein Fallahi, Mohammad Moradi-Shahrbabak, Rostam Abdollahi-Arpanahi, Majid Khansefid, Genomic measures of inbreeding coefficients and genome-wide scan for runs of homozygosity islands in Iranian river buffalo, Bubalus bubalis, BMC Genetics, 10.1186/s12863-020-0824-y, 21, 1, (2020).
- Liangyu Shi, Ligang Wang, Jiaxin Liu, Tianyu Deng, Hua Yan, Longchao Zhang, Xin Liu, Hongmei Gao, Xinhua Hou, Lixian Wang, Fuping Zhao, Estimation of inbreeding and identification of regions under heavy selection based on runs of homozygosity in a Large White pig population, Journal of Animal Science and Biotechnology, 10.1186/s40104-020-00447-0, 11, 1, (2020).
- Elisa Peripolli, Christian Reimer, Ngoc-Thuy Ha, Johannes Geibel, Marco Antonio Machado, João Cláudio do Carmo Panetto, Andréa Alves do Egito, Fernando Baldi, Henner Simianer, Marcos Vinícius Gualberto Barbosa da Silva, Genome-wide detection of signatures of selection in indicine and Brazilian locally adapted taurine cattle breeds using whole-genome re-sequencing data, BMC Genomics, 10.1186/s12864-020-07035-6, 21, 1, (2020).
- Giuseppina Schiavo, Samuele Bovo, Francesca Bertolini, Stefania Dall'Olio, Leonardo Nanni Costa, Silvia Tinarelli, Maurizio Gallo, Luca Fontanesi, Runs of homozygosity islands in Italian cosmopolitan and autochthonous pig breeds identify selection signatures in the porcine genome, Livestock Science, 10.1016/j.livsci.2020.104219, (104219), (2020).
- M. H. Fallahi, H. Moradi Shahrbabak, M. Moradi Shahrbabak, R. Abdollahi Arpanahi, S. Gholami, Assessment of Genetic Diversity in Azerbaijani Buffalo Population in Iran Based on Runs of Homozygosity Stretches, Russian Journal of Genetics, 10.1134/S102279542010004X, 56, 10, (1224-1231), (2020).
- Tomasz Szmatoła, Igor Jasielczuk, Ewelina Semik‐Gurgul, Magdalena Szyndler‐Nędza, Tadeusz Blicharski, Karolina Szulc, Ewa Skrzypczak, Artur Gurgul, Detection of runs of homozygosity in conserved and commercial pig breeds in Poland, Journal of Animal Breeding and Genetics, 10.1111/jbg.12482, 137, 6, (571-580), (2020).
- F. Bertolini, G. Schiavo, S. Bovo, M. T. Sardina, S. Mastrangelo, S. Dall’Olio, B. Portolano, L. Fontanesi, Comparative selection signature analyses identify genomic footprints in Reggiana cattle, the traditional breed of the Parmigiano-Reggiano cheese production system, animal, 10.1017/S1751731119003318, (1-12), (2020).
- G. Schiavo, S. Bovo, F. Bertolini, S. Tinarelli, S. Dall’Olio, L. Nanni Costa, M. Gallo, L. Fontanesi, Comparative evaluation of genomic inbreeding parameters in seven commercial and autochthonous pig breeds, animal, 10.1017/S175173111900332X, (1-11), (2020).
- S. P. Dixit, Sanjeev Singh, Indrajit Ganguly, Avnish Kumar Bhatia, Anurodh Sharma, N. Anand Kumar, Ajay Kumar Dang, S. Jayakumar, Genome-Wide Runs of Homozygosity Revealed Selection Signatures in Bos indicus, Frontiers in Genetics, 10.3389/fgene.2020.00092, 11, (2020).
- Oscar Aramburu, Francisco Ceballos, Adrián Casanova, Alan Le Moan, Jakob Hemmer-Hansen, Dorte Bekkevold, Carmen Bouza, Paulino Martínez, Genomic Signatures After Five Generations of Intensive Selective Breeding: Runs of Homozygosity and Genetic Diversity in Representative Domestic and Wild Populations of Turbot (Scophthalmus maximus), Frontiers in Genetics, 10.3389/fgene.2020.00296, 11, (2020).
- Grazyella M. Yoshida, Pablo Cáceres, Rodrigo Marín-Nahuelpi, Ben F. Koop, José M. Yáñez, Estimates of Autozygosity Through Runs of Homozygosity in Farmed Coho Salmon, Genes, 10.3390/genes11050490, 11, 5, (490), (2020).
- Michela Ablondi, Christos Dadousis, Matteo Vasini, Susanne Eriksson, Sofia Mikko, Alberto Sabbioni, Genetic Diversity and Signatures of Selection in a Native Italian Horse Breed Based on SNP Data, Animals, 10.3390/ani10061005, 10, 6, (1005), (2020).
- K.A. Saravanan, Manjit Panigrahi, Harshit Kumar, Subhashree Parida, Bharat Bhushan, G.K. Gaur, Pushpendra Kumar, Triveni Dutt, B.P. Mishra, R.K. Singh, Genome-wide assessment of genetic diversity, linkage disequilibrium and haplotype block structure in Tharparkar cattle breed of India, Animal Biotechnology, 10.1080/10495398.2020.1796696, (1-15), (2020).
- Enrico Mancin, Michela Ablondi, Roberto Mantovani, Giuseppe Pigozzi, Alberto Sabbioni, Cristina Sartori, Genetic Variability in the Italian Heavy Draught Horse from Pedigree Data and Genomic Information, Animals, 10.3390/ani10081310, 10, 8, (1310), (2020).
- Huiwen Zhan, Saixian Zhang, Kaili Zhang, Xia Peng, Shengsong Xie, Xinyun Li, Shuhong Zhao, Yunlong Ma, Genome-Wide Patterns of Homozygosity and Relevant Characterizations on the Population Structure in Piétrain Pigs, Genes, 10.3390/genes11050577, 11, 5, (577), (2020).
- Guoyao Zhao, Tianliu Zhang, Yuqiang Liu, Zezhao Wang, Lei Xu, Bo Zhu, Xue Gao, Lupei Zhang, Huijiang Gao, George E. Liu, Junya Li, Lingyang Xu, Genome-Wide Assessment of Runs of Homozygosity in Chinese Wagyu Beef Cattle, Animals, 10.3390/ani10081425, 10, 8, (1425), (2020).
- R. Meyermans, W. Gorssen, K. Wijnrocx, J. A. Lenstra, P. Vellema, N. Buys, S. Janssens, Unraveling the genetic diversity of Belgian Milk Sheep using medium‐density SNP genotypes, Animal Genetics, 10.1111/age.12891, 51, 2, (258-265), (2019).
- Elisa Peripolli, Nedenia Bonvino Stafuzza, Sabrina Thaise Amorim, Marcos Vinícius Antunes Lemos, Laís Grigoletto, Sabrina Kluska, José Bento Sterman Ferraz, Joanir Pereira Eler, Elisângela Chicaroni Mattos, Fernando Baldi, Genome‐wide scan for runs of homozygosity in the composite Montana Tropical® beef cattle, Journal of Animal Breeding and Genetics, 10.1111/jbg.12428, 137, 2, (155-165), (2019).
- Lingyang Xu, Guoyao Zhao, Liu Yang, Bo Zhu, Yan Chen, Lupei Zhang, Xue Gao, Huijiang Gao, George E. Liu, Junya Li, Genomic Patterns of Homozygosity in Chinese Local Cattle, Scientific Reports, 10.1038/s41598-019-53274-3, 9, 1, (2019).
- Alexandra L. DeCandia, Kristin E. Brzeski, Elizabeth Heppenheimer, Catherine V. Caro, Glauco Camenisch, Peter Wandeler, Carlos Driscoll, Bridgett M. vonHoldt, Urban colonization through multiple genetic lenses: The city‐fox phenomenon revisited, Ecology and Evolution, 10.1002/ece3.4898, 9, 4, (2046-2060), (2019).
- T.R. Carthy, J. McCarthy, D.P. Berry, A mating advice system in dairy cattle incorporating genomic information, Journal of Dairy Science, 10.3168/jds.2019-16283, (2019).
- Tomasz Szmatoła, Artur Gurgul, Igor Jasielczuk, Tomasz Ząbek, Katarzyna Ropka-Molik, Zygmunt Litwińczuk, Monika Bugno-Poniewierska, A Comprehensive Analysis of Runs of Homozygosity of Eleven Cattle Breeds Representing Different Production Types, Animals, 10.3390/ani9121024, 9, 12, (1024), (2019).
- Tatiana Deniskova, Arsen Dotsev, Eugenia Lushihina, Alexey Shakhin, Elisabeth Kunz, Ivica Medugorac, Henry Reyer, Klaus Wimmers, Negar Khayatzadeh, Johann Sölkner, Alexander Sermyagin, Asankadyr Zhunushev, Gottfried Brem, Natalia Zinovieva, Population Structure and Genetic Diversity of Sheep Breeds in the Kyrgyzstan, Frontiers in Genetics, 10.3389/fgene.2019.01311, 10, (2019).
- Alejandro Amaya, Rodrigo Martínez, Mario Cerón-Muñoz, Population structure and genetic diversity in Colombian Simmental cattle, Tropical Animal Health and Production, 10.1007/s11250-019-02111-w, (2019).
- undefined Xie, undefined Shi, undefined Liu, undefined Deng, undefined Wang, undefined Liu, undefined Zhao, Genome-Wide Scan for Runs of Homozygosity Identifies Candidate Genes in Three Pig Breeds, Animals, 10.3390/ani9080518, 9, 8, (518), (2019).
- Supriya Chhotaray, Manjit Panigrahi, Dhan Pal, Sheikh Firdous Ahmad, V. Bhanuprakash, Harshit Kumar, Subhashree Parida, Bharat Bhushan, G. K. Gaur, B. P. Mishra, R. K. Singh, Genome-wide estimation of inbreeding coefficient, effective population size and haplotype blocks in Vrindavani crossbred cattle strain of India, Biological Rhythm Research, 10.1080/09291016.2019.1600266, (1-14), (2019).
- Seyed Mohammad Ghoreishifar, Hossein Moradi-Shahrbabak, Nahid Parna, Pourya Davoudi, Majid Khansefid, Linkage disequilibrium and within-breed genetic diversity in Iranian Zandi sheep, Archives Animal Breeding, 10.5194/aab-62-143-2019, 62, 1, (143-151), (2019).
- Gertrud Grilz-Seger, Matjaz Mesarič, Marko Cotman, Markus Neuditschko, Thomas Druml, Gottfried Brem, Runs of Homozygosity and Population History of Three Horse Breeds With Small Population Size, Journal of Equine Veterinary Science, 10.1016/j.jevs.2018.09.004, 71, (27-34), (2018).
- Mehrnush Forutan, Saeid Ansari Mahyari, Christine Baes, Nina Melzer, Flavio Schramm Schenkel, Mehdi Sargolzaei, Inbreeding and runs of homozygosity before and after genomic selection in North American Holstein cattle, BMC Genomics, 10.1186/s12864-018-4453-z, 19, 1, (2018).
- Salvatore Mastrangelo, Elena Ciani, Paolo Ajmone Marsan, Alessandro Bagnato, Luca Battaglini, Riccardo Bozzi, Antonello Carta, Gennaro Catillo, Martino Cassandro, Sara Casu, Roberta Ciampolini, Paola Crepaldi, Mariasilvia D’Andrea, Rosalia Di Gerlando, Luca Fontanesi, Maria Longeri, Nicolò P. Macciotta, Roberto Mantovani, Donata Marletta, Donato Matassino, Marcello Mele, Giulio Pagnacco, Camillo Pieramati, Baldassare Portolano, Francesca M. Sarti, Marco Tolone, Fabio Pilla, Conservation status and historical relatedness of Italian cattle breeds, Genetics Selection Evolution, 10.1186/s12711-018-0406-x, 50, 1, (2018).
- Elisa Peripolli, Julia Metzger, Marcos Vinícius Antunes de Lemos, Nedenia Bonvino Stafuzza, Sabrina Kluska, Bianca Ferreira Olivieri, Fabieli Louise Braga Feitosa, Mariana Piatto Berton, Fernando Brito Lopes, Danísio Prado Munari, Raysildo Barbosa Lôbo, Cláudio de Ulhoa Magnabosco, Fernando Di Croce, Jason Osterstock, Sue Denise, Angélica Simone Cravo Pereira, Fernando Baldi, Autozygosity islands and ROH patterns in Nellore lineages: evidence of selection for functionally important traits, BMC Genomics, 10.1186/s12864-018-5060-8, 19, 1, (2018).
- A. Cesarani, S. Sorbolini, A. Criscione, S. Bordonaro, G. Pulina, G. Battacone, D. Marletta, G. Gaspa, N. P. P. Macciotta, Genome‐wide variability and selection signatures in Italian island cattle breeds, Animal Genetics, 10.1111/age.12697, 49, 5, (371-383), (2018).
- S. Mastrangelo, E. Ciani, M. T. Sardina, G. Sottile, F. Pilla, B. Portolano, Runs of homozygosity reveal genome‐wide autozygosity in Italian sheep breeds, Animal Genetics, 10.1111/age.12634, 49, 1, (71-81), (2018).
- Evelyn T. Todd, Simon Y. W. Ho, Peter C. Thomson, Rachel A. Ang, Brandon D. Velie, Natasha A. Hamilton, Founder-specific inbreeding depression affects racing performance in Thoroughbred horses, Scientific Reports, 10.1038/s41598-018-24663-x, 8, 1, (2018).
- V. Palombo, M. Milanesi, S. Sgorlon, S. Capomaccio, M. Mele, E. Nicolazzi, P. Ajmone-Marsan, F. Pilla, B. Stefanon, M. D'Andrea, Genome-wide association study of milk fatty acid composition in Italian Simmental and Italian Holstein cows using single nucleotide polymorphism arrays, Journal of Dairy Science, 10.3168/jds.2018-14413, 101, 12, (11004-11019), (2018).
- Marty Kardos, Pirmin Nietlisbach, Philip W. Hedrick, How should we compare different genomic estimates of the strength of inbreeding depression?, Proceedings of the National Academy of Sciences, 10.1073/pnas.1714475115, 115, 11, (E2492-E2493), (2018).
- Elisa Peripolli, Nedenia Bonvino Stafuzza, Danísio Prado Munari, André Luís Ferreira Lima, Renato Irgang, Marco Antonio Machado, João Cláudio do Carmo Panetto, Ricardo Vieira Ventura, Fernando Baldi, Marcos Vinícius Gualberto Barbosa da Silva, Assessment of runs of homozygosity islands and estimates of genomic inbreeding in Gyr (Bos indicus) dairy cattle, BMC Genomics, 10.1186/s12864-017-4365-3, 19, 1, (2018).
- B. Hillestad, J. A. Woolliams, S. A. Boison, H. Grove, T. Meuwissen, D. I. Våge, G. Klemetsdal, Detection of runs of homozygosity in Norwegian Red: Density, criteria and genotyping quality control, Acta Agriculturae Scandinavica, Section A — Animal Science, 10.1080/09064702.2018.1501088, 67, 3-4, (107-116), (2018).
- Pattarapol Sumreddee, Sajjad Toghiani, El Hamidi Hay, Andrew Roberts, Samuel E Agrrey, Romdhane Rekaya, Inbreeding depression in line 1 Hereford cattle population using pedigree and genomic information1, Journal of Animal Science, 10.1093/jas/sky385, (2018).
- Arnaldo Basso Rebelato, Alexandre Rodrigues Caetano, Runs of homozygosity for autozygosity estimation and genomic analysis in production animals, Pesquisa Agropecuária Brasileira, 10.1590/s0100-204x2018000900001, 53, 9, (975-984), (2018).
- Robert B. Onzima, Maulik R. Upadhyay, Harmen P. Doekes, Luiz. F. Brito, Mirte Bosse, Egbert Kanis, Martien A. M. Groenen, Richard P. M. A. Crooijmans, Genome-Wide Characterization of Selection Signatures and Runs of Homozygosity in Ugandan Goat Breeds, Frontiers in Genetics, 10.3389/fgene.2018.00318, 9, (2018).
- Mija Jansson, Linda Laikre, Pedigree data indicate rapid inbreeding and loss of genetic diversity within populations of native, traditional dog breeds of conservation concern, PLOS ONE, 10.1371/journal.pone.0202849, 13, 9, (e0202849), (2018).
- Kwondo Kim, Jaehoon Jung, Kelsey Caetano-Anollés, Samsun Sung, DongAhn Yoo, Bong-Hwan Choi, Hyung-Chul Kim, Jin-Young Jeong, Yong-Min Cho, Eung-Woo Park, Tae-Jeong Choi, Byoungho Park, Dajeong Lim, Heebal Kim, Artificial selection increased body weight but induced increase of runs of homozygosity in Hanwoo cattle, PLOS ONE, 10.1371/journal.pone.0193701, 13, 3, (e0193701), (2018).
- Daniel Goszczynski, Antonio Molina, Ester Terán, Hernán Morales-Durand, Pablo Ross, Hao Cheng, Guillermo Giovambattista, Sebastián Demyda-Peyrás, Runs of homozygosity in a selected cattle population with extremely inbred bulls: Descriptive and functional analyses revealed highly variable patterns, PLOS ONE, 10.1371/journal.pone.0200069, 13, 7, (e0200069), (2018).
- Thomas Druml, Markus Neuditschko, Gertrud Grilz-Seger, Michaela Horna, Anne Ricard, Matjaz Mesarič, Marco Cotman, Hubert Pausch, Gottfried Brem, Population Networks Associated with Runs of Homozygosity Reveal New Insights into the Breeding History of the Haflinger Horse, Journal of Heredity, 10.1093/jhered/esx114, 109, 4, (384-392), (2017).
- Alexandra Blant, Michelle Kwong, Zachary A. Szpiech, Trevor J. Pemberton, Weighted likelihood inference of genomic autozygosity patterns in dense genotype data, BMC Genomics, 10.1186/s12864-017-4312-3, 18, 1, (2017).
- Ino Curik, Maja Ferenčaković, Johann Sölkner, Genomic dissection of inbreeding depression: a gate to new opportunities, Revista Brasileira de Zootecnia, 10.1590/s1806-92902017000900010, 46, 9, (773-782), (2017).
- Marina Solé, Ann-Stephan Gori, Pierre Faux, Amandine Bertrand, Frédéric Farnir, Mathieu Gautier, Tom Druet, Age-based partitioning of individual genomic inbreeding levels in Belgian Blue cattle, Genetics Selection Evolution, 10.1186/s12711-017-0370-x, 49, 1, (2017).
- Heidi Signer-Hasler, Alexander Burren, Markus Neuditschko, Mirjam Frischknecht, Dorian Garrick, Christian Stricker, Birgit Gredler, Beat Bapst, Christine Flury, Population structure and genomic inbreeding in nine Swiss dairy cattle populations, Genetics Selection Evolution, 10.1186/s12711-017-0358-6, 49, 1, (2017).
- Luiz F. Brito, James W. Kijas, Ricardo V. Ventura, Mehdi Sargolzaei, Laercio R. Porto-Neto, Angela Cánovas, Zeny Feng, Mohsen Jafarikia, Flávio S. Schenkel, Genetic diversity and signatures of selection in various goat breeds revealed by genome-wide SNP markers, BMC Genomics, 10.1186/s12864-017-3610-0, 18, 1, (2017).
- Salvatore Mastrangelo, Marco Tolone, Maria T. Sardina, Gianluca Sottile, Anna M. Sutera, Rosalia Di Gerlando, Baldassare Portolano, Genome-wide scan for runs of homozygosity identifies potential candidate genes associated with local adaptation in Valle del Belice sheep, Genetics Selection Evolution, 10.1186/s12711-017-0360-z, 49, 1, (2017).
- Deirdre C. Purfield, Sinead McParland, Eamon Wall, Donagh P. Berry, The distribution of runs of homozygosity and selection signatures in six commercial meat sheep breeds, PLOS ONE, 10.1371/journal.pone.0176780, 12, 5, (e0176780), (2017).
- E. Peripolli, D. P. Munari, M. V. G. B. Silva, A. L. F. Lima, R. Irgang, F. Baldi, Runs of homozygosity: current knowledge and applications in livestock, Animal Genetics, 10.1111/age.12526, 48, 3, (255-271), (2016).
- Gabriele Marras, Attilio Rossoni, Hermann Schwarzenbacher, Stefano Biffani, Filippo Biscarini, Ezequiel L. Nicolazzi, zanardi: an open‐source pipeline for multiple‐species genomic analysis of SNP array data, Animal Genetics, 10.1111/age.12485, 48, 1, (121-121), (2016).
- Arianna Manunza, Antonia Noce, Juan Manuel Serradilla, Félix Goyache, Amparo Martínez, Juan Capote, Juan Vicente Delgado, Jordi Jordana, Eva Muñoz, Antonio Molina, Vincenzo Landi, Agueda Pons, Valentin Balteanu, Amadou Traoré, Montse Vidilla, Manuel Sánchez-Rodríguez, Armand Sànchez, Tainã Figueiredo Cardoso, Marcel Amills, A genome-wide perspective about the diversity and demographic history of seven Spanish goat breeds, Genetics Selection Evolution, 10.1186/s12711-016-0229-6, 48, 1, (2016).
- A. Gurgul, T. Szmatoła, P. Topolski, I. Jasielczuk, K. Żukowski, M. Bugno-Poniewierska, The use of runs of homozygosity for estimation of recent inbreeding in Holstein cattle, Journal of Applied Genetics, 10.1007/s13353-016-0337-6, 57, 4, (527-530), (2016).
- Karim Karimi, Ali Esmailizadeh Koshkoiyeh, Masood Asadi Fozi, Laercio R. Porto-Neto, Cedric Gondro, Prioritization for conservation of Iranian native cattle breeds based on genome-wide SNP data, Conservation Genetics, 10.1007/s10592-015-0762-9, 17, 1, (77-89), (2015).
- Qianqian Zhang, Mario PL Calus, Bernt Guldbrandtsen, Mogens S Lund, Goutam Sahana, Estimation of inbreeding using pedigree, 50k SNP chip genotypes and full sequence data in three cattle breeds, BMC Genetics, 10.1186/s12863-015-0227-7, 16, 1, (2015).
- Alberto Cesarani, Giustino Gaspa, Alfredo Pauciullo, Lorenzo Degano, Daniele Vicario, Nicolò P. P. Macciotta, Genome‐wide analysis of homozygosity regions in european simmental bulls, Journal of Animal Breeding and Genetics, 10.1111/jbg.12502, 0, 0, (undefined).
