Runs of Homozygosity Provide a Genome Landscape Picture of Inbreeding and Genetic History of European Autochthonous and Commercial Pig Breeds
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FULL PAPER doi: 10.1111/age.13045 Runs of homozygosity provide a genome landscape picture of inbreeding and genetic history of European autochthonous and commercial pig breeds † † ‡ § G. Schiavo* , S. Bovo* ,M.Munoz˜ , A. Ribani* , E. Alves , J. P. Araujo´ , R. Bozzi , ¶ † †† † ‡‡ §§ M. Candek-Potokarˇ , R. Charneca**, A. I. Fernandez ,M.Gallo ,F.Garcı´a ,D.Karolyi ,G.Kusecˇ , ¶¶ † ††† ‡‡‡ J. M. Martins**, M.-J. Mercat ,Y.Nu´nez˜ , R. Quintanilla***, C.ˇ Radovic´ , V. Razmaite , §§§ ¶¶¶ †††† † J. Riquet , R. Savic´ , G. Usai****, V. J. Utzeri* , C. Zimmer , C. Ovilo and L. Fontanesi* *Department of Agricultural and Food Sciences, Division of Animal Sciences, University of Bologna, Viale Giuseppe Fanin 46, Bologna 40127, † ‡ Italy. Departamento Mejora Genetica´ Animal, INIA, Crta. de la Coruna,˜ km. 7,5, Madrid 28040, Spain. Centro de Investigac¸ao˜ de Montanha § (CIMO), Instituto Politecnico´ de Viana do Castelo, Escola Superior Agraria,´ Refoios´ do Lima, Ponte de Lima 4990-706, Portugal. DAGRI - ¶ Animal Science Division, Universita` di Firenze, Via delle Cascine 5, Firenze 50144, Italy. Kmetijski Institutˇ Slovenije, Hacquetova 17, Ljubljana SI-1000, Slovenia. **Instituto de Cienciasˆ Agrarias´ e Ambientais Mediterranicas,ˆ Universidade de Evora,´ Polo da Mitra, Apartado 94, Evora´ †† ‡‡ 7006-554, Portugal. Associazione Nazionale Allevatori Suini, Via Nizza 53, Rome 00198, Italy. Department of Animal Science, Faculty of §§ Agriculture, University of Zagreb, Svetosimunskaˇ c. 25, Zagreb 10000, Croatia. Faculty of Agrobiotechnical Sciences, University of Osijek, ¶¶ Vladimira Preloga 1, Osijek 31000, Croatia. IFIP Institut du porc, La Motte au Vicomte, BP 35104, Le Rheu Cedex 35651, France. ††† ***Programa de Genetica´ y Mejora Animal, IRTA, Torre Marimon, Caldes de Montbui, Barcelona 08140, Spain. Department of Pig Breeding ‡‡‡ and Genetics, Institute for Animal Husbandry, Belgrade-Zemun 11080, Serbia. Animal Science Institute, Lithuanian University of Health §§§ Sciences, Baisogala 82317, Lithuania. GenPhySE, Universite´ de Toulouse, INRA, Chemin de Borde-Rouge 24, Auzeville Tolosane, Castanet ¶¶¶ Tolosan 31326, France. Faculty of Agriculture, University of Belgrade, Nemanjina 6, Belgrade-Zemun 11080, Serbia. ****Agris Sardegna, †††† Loc. Bonassai, Sassari 07100, Italy. Bauerliche¨ Erzeugergemeinschaft Schwabisch¨ Hall, Haller Str. 20, Wolpertshausen 74549, Germany. Summary ROHs are long stretches of DNA homozygous at each polymorphic position. The proportion of genome covered by ROHs and their length are indicators of the level and origin of inbreeding. Frequent common ROHs within the same population define ROH islands and indicate hotspots of selection. In this work, we investigated ROHs in a total of 1131 pigs from 20 European local pig breeds and in three cosmopolitan breeds, genotyped with the GGP Porcine HD Genomic Profiler. PLINK software was used to identify ROHs. Size classes and genomic inbreeding parameters were evaluated. ROH islands were defined by evaluating different thresholds of homozygous SNP frequency. A functional overview of breed-specific ROH islands was obtained via over- representation analyses of GO biological processes. Mora Romagnola and Turopolje breeds had the largest proportions of genome covered with ROH (~1003 and ~955 Mb respectively), whereas Nero Siciliano and Sarda breeds had the lowest proportions (~207 and 247 Mb respectively). The highest proportion of long ROH (>16 Mb) was in Apulo-Calabrese, Mora Romagnola and Casertana. The largest number of ROH islands was identified in the Italian Landrace (n = 32), Cinta Senese (n = 26) and Lithuanian White Old Type (n = 22) breeds. Several ROH islands were in regions encompassing genes known to affect morphological traits. Comparative ROH structure analysis among breeds indicated the similar genetic structure of local breeds across Europe. This study contributed to understanding of the genetic history of the investigated pig breeds and provided information to manage these pig genetic resources. Keywords autozygosity, population genomics, selection signature, single nucleotide polymorphism, Sus scrofa Address for correspondence Introduction L. Fontanesi, Department of Agricultural and Food Sciences, Division of Conservation programs of animal genetic resources, mainly Animal Sciences, University of Bologna, Viale Giuseppe Fanin 46, Bologna 40127, Italy. E-mail: [email protected] constituted by numerous autochthonous breeds in all Accepted for publication 15 January 2021 species, are usually challenged by their small effective © 2021 Stichting International Foundation for Animal Genetics, 52, 155–170 155 156 Schiavo et al. population size which, in turn, tends to increase inbreeding et al. 2017; Bertolini et al. 2018; Grilz-Seger et al. 2018; and reduce genetic variability (Charlesworth & Willis Mastrangelo et al. 2018; Peripolli et al. 2018), including 2009). Inbreeding depression is considered the result of the pig (Zhang et al. 2018; Gorssen et al. 2020; Schiavo the increased level of autozygosity. Pedigree information is et al. 2020a). traditionally used to calculate the inbreeding coefficient A lot of different pig breeds have been developed (FPED), defined as the probability that in a diploid individual, through the combined action of artificial directional the maternal and paternal derived alleles at a randomly selection and natural pressures that have contributed to selected locus are identical by descent (Wright 1922). This shaping a large reservoir of genetic diversity within the definition is equivalent to considering FPED as the proportion Sus scrofa species (Porter 1993). A large fraction of these of autozygosity of an individual’s genome. Then, the level of genetic resources is, however, constituted by autochtho- inbreeding of a population is expressed by averaging all FPED nous breeds of small population size, usually well adapted individual values. The reliability of FPED calculated in to their local agro-climatic and environmental conditions autochthonous breeds is in general lower than what it is but less productive, compared with cosmopolitan breeds or possible to obtain for animals in commercial selection lines. Conservation programs for these breeds, some of nuclei. This is mainly due to incomplete registration and which are considered unexplored genetic resources, have incorrect recording of all mating events derived by the different levels of managing actions that range from extensive production systems in which local breeds are advanced herd book structures with specific breeding and usually raised (Gomez-Raya et al. 2008; Kios et al. 2012). In selection plans to preliminary voluntary farmer-based herd addition, it is clear that some assumptions used to calculate books or primitive conservation programs (Candek-Potokarˇ this pedigree-based coefficient are not correct and they are & Nieto 2019). We recently analyzed major and candidate used as approximations in the methods of calculations: (i) gene markers in 20 autochthonous European pig breeds all founder animals of the base population are expected to from several different countries and obtained preliminary be unrelated, but this condition cannot be evaluated and it population structure results (Munoz˜ et al. 2018) that were is usually not respected; (ii) recombinant events occurring refined using SNP array information (Munoz˜ et al. 2019) during meiosis mix equally the individual’s paternal and and whole genome resequencing data (Bovo et al. 2020a, maternal haploid genome copies, but this condition mimics b). Genome-wide data indicated that the average persis- only average events and not what actually happens in each tence and strength of LD between markers and SNP-based specific meiosis; and (iii) there are no selection biases on any effective population size varied among breeds depending on parts of the genome, but this assumption is not respected the genetic structures and history of these breeds that had considering that directional artificial selection and natural experienced different genetic events (e.g. admixture, bot- selection play important roles in shaping the genome of tlenecks and genetic drift). Selection signatures were also many domestic animal breeds (Leutenegger et al. 2003; obtained using FST statistics by analyzing SNP chip Wang 2016; Knief et al. 2017). genotyping and sequencing data (Munoz˜ et al. 2019; Bovo Genome-wide analyses, usually based on SNP arrays, et al. 2020a). Genomic inbreeding analyses in these breeds can be used to estimate the level of autozygosity of an could be used as additional information to refine their animal genome by directly interrogating the genotype conservation programs, by controlling the level of autozy- status at thousands of polymorphic sites (Kristensen et al. gosity, and identify appropriate strategies to control 2010). The proportion of the genome covered by ROHs of inbreeding level and infer other population structures or a certain minimal length has been considered one of the features, such as breed-specific or subpopulation homozy- most precise estimations of the level of autozygosity, gosity hotspots. providing a measure of genomic inbreeding (FROH; Peripolli In this study, we analyzed the same 20 European et al. 2017). ROHs are defined as continuous chromosome autochthonous pig breeds from nine different countries stretches in which all loci have a homozygous genotype (Croatia, France, Germany, Italy, Lithuania, Portugal, (Gibson et al. 2006). Some ROH characteristics in a Serbia, Slovenia and Spain) and three