Diversity across major and candidate genes in European local pig breeds

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Abstract

The aim of this work was to analyse the distribution of causal and candidate mutations associated to relevant productive traits in twenty local European pig breeds. Also, the potential of the SNP panel employed for elucidating the genetic structure and relationships among breeds was evaluated. Most relevant genes and mutations associated with pig morphological, productive, meat quality, reproductive and disease resistance traits were prioritized and analyzed in a maximum of 47 blood samples from each of the breeds (Alentejana, Apulo-Calabrese, Basque, Bísara, Majorcan Black, Black Slavonian (Crna slavonska), Casertana, Cinta Senese, Gascon, Iberian, Krškopolje (Krškopoljski), Lithuanian indigenous wattle, Lithuanian White Old Type, Mora Romagnola, Moravka, Nero Siciliano, Sarda, Schwäbisch-Hällisches Schwein (Swabian Hall pig), Swallow-Bellied Mangalitsa and Turopolje). We successfully analyzed allelic variation in 39 polymorphisms, located in 33 candidate genes. Results provide relevant information regarding genetic diversity and segregation of SNPs associated to production and quality traits. Coat color and morphological trait-genes that show low level of segregation, and fixed SNPs may be useful for traceability. On the other hand, we detected SNPs which may be useful for association studies as well as breeding programs. For instance, we observed predominance of alleles that might be unfavorable for disease resistance and boar taint in most breeds and segregation of many alleles involved in meat quality, fatness and growth traits. Overall, these findings provide a detailed catalogue of segregating candidate SNPs in 20 European local pig breeds that may be useful for traceability purposes, for association studies and for breeding schemes. Population genetic analyses based on these candidate genes are able to uncover some clues regarding the hidden genetic substructure of these populations, as the extreme genetic closeness between Iberian and Alentejana breeds and an uneven admixture of the breeds studied. The results are in agreement with available knowledge regarding breed history and management, although largest panels of neutral markers should be employed to get a deeper understanding of the population’s structure and relationships.

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J Fujii, Ciara O'Brien, F. Zorzato … (1991)

Malignant hyperthermia (MH) causes neurological, liver, and kidney damage and death in humans and major economic losses in the swine industry. A single point mutation in the porcine gene for the skeletal muscle ryanodine receptor (ryr1) was found to be correlated with MH in five major breeds of lean, heavily muscled swine. Haplotyping suggests that the mutation in all five breeds has a common origin. Assuming that this is the causal mutation for MH, the development of a noninvasive diagnostic test will provide the basis for elimination of the MH gene or its controlled inclusion in swine breeding programs.

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A mutation in PRKAG3 associated with excess glycogen content in pig skeletal muscle.

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A high proportion of purebred Hampshire pigs carries the dominant RN- mutation, which causes high glycogen content in skeletal muscle. The mutation has beneficial effects on meat content but detrimental effects on processing yield. Here, it is shown that the mutation is a nonconservative substitution (R200Q) in the PRKAG3 gene, which encodes a muscle-specific isoform of the regulatory gamma subunit of adenosine monophosphate-activated protein kinase (AMPK). Loss-of-function mutations in the homologous gene in yeast (SNF4) cause defects in glucose metabolism, including glycogen storage. Further analysis of the PRKAG3 signaling pathway may provide insights into muscle physiology as well as the pathogenesis of noninsulin-dependent diabetes mellitus in humans, a metabolic disorder associated with impaired glycogen synthesis.

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Contrasting Mode of Evolution at a Coat Color Locus in Wild and Domestic Pigs

Meiying Fang, Greger Larson, Lucia Ribeiro … (2009)

Introduction The sizes, shapes, and colors among domestic animals vary significantly more than that of their wild counterparts, often reflecting variation normally associated with genus or family level divergence [1]. Domestication therefore provides an ideal model to test numerous evolutionary questions including the relationship between molecular and morphological change, how the intensification of the relationship between humans and wild plants and animals have altered both players' genetic and phenotypic constitutions, and whether changes associated with domestication resulted primarily from a release of natural selection pressure, selection on standing genetic variation present in the wild ancestor, or positive selection on novel mutations that have occurred subsequent to domestication. Coat color variation in domestic animals is of considerable interest in this respect considering that it can be traced back to at least 5,000 years before present when it was documented by administrative officers who recorded the coat color of livestock during the UR III dynasty in Mesopotamia [2]. Modern domestic animal species display a bewildering diversity in coat color, and the melanocortin receptor 1 (MC1R) locus is most consistently polymorphic, having been previously documented and associated with coat color variation in horses, cattle, foxes, pigs, sheep, dogs, and chickens [3]–[10]. MC1R is a G protein-coupled receptor that is primarily expressed in melanocytes and plays a key role in melanogenesis by determining the switch between production of red/yellow pheomelanin and dark eumelanin [11]. The binding of melanocyte stimulating hormone (MSH) to MC1R induces synthesis of eumelanin, whereas in the absence of MC1R signaling, melanocytes produce only pheomelanin. Loss-of-function mutations are therefore associated with recessive red coat color, whereas dominant black coloring is linked with mutations causing constitutive activation of MC1R signaling. We have previously described the molecular basis for an allelic series at the classical Extension locus (equivalent to MC1R) in pigs [6],[7],[12]. The wild-type (E+ ) allele allows full expression of both pheomelanin and eumelanin. The dominant black color results from two different mutations, each of which evolved independently in Asia and Europe. The ED1 allele is Asian in origin and is associated with an L102P missense mutation, and ED2 is European and associated with a D124N substitution. The recessive red allele (e) possesses two missense mutations A164V and A243T, though it is not clear if one or both of these are responsible for the phenotype. The most interesting allele is EP which causes black spotting on a red or white background. This allele evolved from ED2 and possesses, in addition to the D124N substitution for dominant black coloring, a two base pair insertion at codon 22. Two C nucleotides have been inserted in a stretch of six Cs, thus extending a short mononucleotide repeat. The resulting frameshift is expected to cause a uniform red pigmentation due to the complete loss of MC1R signaling, but because the mononucleotide repeat is somatically unstable, MC1R function in some melanocyte lineages is occasionally restored, resulting in the appearance of black spots [7]. All of these alleles were described from a limited subset of wild and domestic pigs. In order to more fully understand the range of MC1R variations within Sus scrofa, we determined the entire MC1R coding sequence (963 bp) within 68 domestic pigs (representing 51 Asian and European breeds) and a total of 15 Chinese and European wild boar, the results of which are described in Tables S1, S2, S3, S4. In addition, one previously published Japanese wild boar sequence [13] was incorporated into the analysis. Results The sampling strategy outlined above resulted in a near doubling of the number of described MC1R alleles from seven to 13, all of which belonged to the five previously described allelic groups. A large proportion of the domestic pigs (60 out of 68) were homozygous at MC1R despite the fact that eight different alleles were identified within domestic pigs (Table S3). This high degree of homozygosity is not surprising given that coat colors have been used as a specific breed characteristic over the past 200 years, and within most populations there has been strong selection for uniformity in coat color as this trait often defines the breed. This screen revealed three new missense mutations in pig MC1R, Val122Ile in the Asian *0202 allele, Ala21Thr in the European *0502 allele and finally Arg166Trp in the European *0503 (Table S2). Since these variants were detected in a few pigs that may carry other coat color mutations we cannot judge if they have an impact on the coat color phenotype and this needs to be further investigated. Until such data become available we assume that they are associated with dominant black color (*0202) and black spotting (*0502 and *0503). All domestic breeds in Europe and China carried mutant MC1R alleles except the Hungarian Mangalica. Though this breed is homozygous for the European wild type MC1R allele, it still possesses a variable coat color phenotype, a fact at least partially explained by allelic segregation at the agouti (ASIP) locus [14]. The EP (black spotting) MC1R allele dominates among European domestic pigs, particularly amongst commercial populations (Table S4). The allele for dominant black color (ED2 ) is more common in local European breeds whereas the allele (e) for recessive red color was only found in the Duroc and Leicoma breeds. One Creole pig carried the Asian ED1 allele for dominant black color, reflecting the introgression of Asian pigs into European stocks that took place during the 18th and 19th century [13]. All tested Chinese pigs carried the ED1 allele for dominant black color. Lastly, three Chinese domestic pigs were heterozygous for the European e or EP alleles, an observation that is most certainly caused by recent introgression of European germplasm into local Chinese breeds. The European, Chinese, and Japanese wild boars all carried wild-type alleles that differ only by synonymous substitutions (Tables S2, S3). All 12 European wild boar carried identical MC1R sequences which were also identical to a previously described European wild boar sequence [13] and to the one present in Mangalica domestic pigs. The complete absence of synonymous substitutions between European wild boar and European domestic pig MC1R sequences supports the notion that the European wild boar experienced a population bottleneck prior to domestication [15],[16]. The higher MC1R diversity within Chinese wild boar relative to European wild boar is also consistent with recent microsatellite data indicating that Asian domestic pigs were derived from a more diverse wild boar population [17]. One Chinese wild boar was heterozygous for the EP allele but this must be the result of gene flow from domestic pigs since the allele is of European origin and differs from native Chinese wild boar alleles by at least two synonymous and two non-synonymous substitutions (Table S2). The amino acid sequence conservation within wild boar is sharply contrasted by the sequence diversity amongst MC1R alleles found within domestic pigs. This is illustrated in Figures 1A and 1B which depict the completely synonymous nature of all seven nucleotide substitutions found among European and Asian wild boar. The figure also shows that all mutations except one detected amongst European and Chinese domestic pigs altered the amino acid sequence, eight are non-synonymous substitutions and one is the frameshift at codon 22 that is widespread among European domestic pigs. The same synonymous substitution was found in both the Chinese domestic allele *0203 and in the Asian wild boar allele *0104 (Figure 1B). 10.1371/journal.pgen.1000341.g001 Figure 1 Amino acid sequence conservation within wild boar is sharply contrasted by the sequence diversity amongst MC1R alleles found within domestic pigs. (A) The observed number of synonymous and non-synonymous substitutions amongst Chinese and European domestic pigs and amongst Chinese and European wild boars; included amongst the “non-synonymous” substitutions is the two base pair insertion associated with the EP allele. The diversity of coat color among domestic pigs is exemplified by the images on the left and contrasted with the camouflaged coat color in the wild boar on the lower right. (B) A Median-joining network of MC1R alleles in Asian and European pigs. All known alleles are represented by circles while squares represent predicted intermediate forms that have not yet been found. Thin black lines placed perpendicular to the lines connecting the individual haplotypes represent single, synonymous changes, and thicker red lines represent non-synonymous changes. The asterisk placed near the two black lines leading to alleles *0104 and *0203 indicates the only instance of an identical mutation at different locations on the tree. Colors inside the circles and squares depict the observed and predicted coat colors associated with a given allele; question marks inside two of the squares indicate that the associated coat color of these intermediate alleles cannot be predicted because they connect alleles that differ by two non-synonymous substitutions. The first two digits in the nomenclature for porcine MC1R alleles alongside the circles indicate the associated coat color phenotype: 01 = wild type, 02 = dominant black, Asian form, 03 = dominant black, European form, 04 = recessive red, and 05 = black spotting. The two last digits are used to distinguish alleles that are associated with the same phenotype. (C) Wild boar sow with piglets in the nest. Note the remarkable camouflage coat color pattern in the piglets. (Photo: Anneli Andersson, Linköping University, Sweden.) The existence of radically different selective pressures acting on MC1R in wild and domestic pigs was demonstrated by an analysis of the relative frequencies of non-synonymous (dN) and synonymous substitutions (dS) (Table 1); a dN/dS ratio higher than 1.0 indicates positive selection while a dN/dS ratio significantly lower than 1.0 provides evidence for purifying selection. The most informative contrasts were those between Asian and Europan wild boars and between Asian and European domestic pigs. The former comparison provided evidence for purifying selection in wild boars since no non-synonymous substitution was observed and the frequency of synonymous substitutions was significantly different from 0 (Z = 2.55, P<0.01). In contrast, the dN/dS ratio was as high as 23.5 for the comparison between Asian and European domestic pigs, ignoring the three synonymous substitutions that distinguish Asian from European alleles but which must have occurred in wild boars prior to domestication (Figure 1B). The excess of non-synonymous substitutions between European and Asian domestic pigs was statistically significant (Z = 2.05; P<0.01) and provided strong support for positive selection. This analysis in fact underestimates the evidence for diversifying selection since the dN/dS analysis did not take into account the frameshift mutation that is widespread among European domestic pigs. 10.1371/journal.pgen.1000341.t001 Table 1 Analysis of the frequency of non-synonymous (dN) and synonymous (dS) substitutions among wild and domestic pigs from Europe and Asia. Comparison n %dN±s.e. %dS±s.e. dN/dS Within populations European wild boar (EWB) 24 0 0 0 European domestic (ED) 89 0.13±0.06 0 ∞ Asian wild boar (AWB) 5 0 1.33±0.51 0 Asian domestic (AD) 42 0.01±0.01 0.04±0.03 0.25 Between populations EWB vs ED 0.18±0.12 0 ∞ AWB vs. AD 0.29±0.20 0.95±0.37 0.31 EWB vs. AWB 0 1.48±0.58 0 ED vs. AD1 0.47±0.23 0.02±0.02 23.5 n = number of sequenced chromosomes as indicated in Table S3; Asian alleles found in European pigs and European alleles found in Asian pigs were excluded from the analysis since they most certainly reflect recent introgressions. 1 The three synonymous substitutions present in both Asian wild boars and Asian domestic pigs (Table S2) were excluded from the analysis in order to restrict the analysis to those substitutions that occurred subsequent to domestication. Furthermore, the large number of non-synonymous substitutions cannot be explained by relaxed selection subsequent to pig domestication. The reason is that the time since domestication (about 10,000 years) is not sufficiently long to accumulate as many mutations that have gone to fixation in domestic populations or the existence of several alleles that differ by multiple steps from the ancestral form. We have previously estimated the time since divergence of European and Asian wild boar populations to about 900,000 years before present based on a 1.2% sequence difference across the entire mitochondrial genome [18]. This is very similar to the recently estimated sequence divergence of about 1.3% for the entire mitochondrial genome between modern humans and Neandertals and the time since divergence of these two mtDNA lineages were estimated at 660,000±140,000 years [19]. Thus, the seven synonymous substitutions observed among Asian and European wild boars have accumulated during hundreds of thousands of years whereas the nine mutations changing the MC1R protein sequence among domestic pigs have accumulated within the last 10,000 years. Thus, we refute relaxed selection as a possible explanation for the fast evolution of MC1R diversity in domestic pigs and conclude that the only reasonable explanation for this plethora of diversity is that humans have cherry-picked novel mutations with favorable phenotypic effects during the course of domestication. A reconstructed evolutionary history of porcine MC1R sequences (Figure 1B) demonstrates not only the pattern of synonymous substitutions (Table S2) that differentiate Asian and European wild boar sequences, but also the fact that domestic pig MC1R alleles are directly derived from wild boar from the same region, a conclusion supported by previous publications that investigated other loci [13],[18],[20]. Discussion The MC1R diversity within Europe and China presented here reveals divergent selection pressures in wild and domestic pigs. A previous study of mtDNA genome sequences derived from European and Asian wild boars indicated that these subspecies diverged well before the advent of domestication [18]. In this study, we identified a total of seven synonymous nucleotide substitutions within MC1R sequences from Asian and European wild boar. The temporally and geographically conserved nature of Sus MC1R amino acid sequence demonstrates that purifying selection is the dominant mode of evolution at this locus in the wild boar because normal MC1R function, which generates a mixture of dark eumelanin and red/yellow pheomelanin, is necessary for a camouflaged coat. MC1R underlies coat color diversity in many natural and domestic populations. This study demonstrates that this diversity cannot be explained by an exceptionally high substitution rate at this locus. Instead, a more likely explanation of this pattern is that though MC1R is a master regulator for melanogenesis, its primary role is restricted to melanocytes. Thus, MC1R mutations can have major effects on coat color phenotypes without causing severe pleiotropic effects on other tissues, a phenomenon that often results from mutations at other coat color loci [21]. Because domestication necessarily involves the separation of animals from their natural environment, the alterations in coat color during animal domestication could have been the result of a relaxation of the selection pressure against non-camouflaged coat. The evidence presented here, however, demonstrates that relaxed selection alone cannot explain the observed MC1R diversity in domestic pigs. The complete lack of non-synonymous substitutions within European and Chinese wild boar (who diverged in the Pleistocene) is contrasted sharply by the nine separate amino acid-altering mutations present within domestic pigs. This pattern implies that naturally occurring mutations that altered camouflaged coat colors were quickly eliminated in the wild, but within a domesticated context, these mutations were prized and positively selected. Having been allowed to proliferate, the new mutated alleles served as templates on which additional mutations occurred (Figure 1B). This conclusion is underscored by the fact that seven of the eight MC1R alleles found in domestic pigs differed by two or more non-synonymous substitutions from the wild-type. In fact, three of the alleles (*0202, *0502 and *0503) differed by as many as three non-synonymous substitutions from the wild-type. We propose that an important component of the selection at coat color loci in domestic animals has been direct selection for non-camouflaged patterns, since the mutated coat colors may have facilitated animal husbandry. The traditional practice of keeping domestic pigs involved allowing them to forage beyond the boundaries of the farm. Possessing a coat color significantly different from the wild type would have made it easier to recognize and keep track of domestic stocks. Furthermore, variant coat color phenotypes may also have been used as markers associated with improved domesticated forms. Finally, the ubiquity of the black spotting caused by the EP allele, may be a result of the universal human penchant to select for and propagate attractive patterns present within the floral and fauna with which humans have a close relationship. Three recent illustrative examples of human preference for novelty include selection for white color in horses [22], the human-mediated spread of white Polynesian tree snails between Polynesian islands [23], and the global proliferation of white grape cultivars, which, like some domestic coat colors, results from the inactivation of a gene necessary for wild type (red) grape coloring [24]. Black coloring is common in both European and Asian domestic pigs but because different allelic substitutions underlie this indistinguishable phenotype, it is clear that there have been independent selective sweeps for separate alleles causing dominant black color in both China and Europe. In China, selection for the L102P substitution has been strong enough to penetrate all 23 breeds representing the six traditional types of Chinese pigs. Similarly, 90% of MC1R sequences found in European domestic pigs carried the D124N missense mutation causing dominant black color. Despite dramatic phenotypic differences between wild and domestic animals, no fixed mutation has yet been identified that distinguishes domesticated and wild forms of a given species. The MC1R locus in pigs approaches such a diagnostic status since only one breed (the Mangalica) out of 51 included in this study carried the wild-type allele. Interestingly, to the best of our knowledge, Mangalica pigs are also the only pigs included in this study that give birth to striped piglets that resemble striped wild boar piglets (Figure 1C). This indicates that normal MC1R signaling is required for the development of stripes in piglets and it may therefore also be important for the development of stripes in other species like the Tiger and Zebra. The striping that occurs in wild boar piglets is most certainly a camouflage pattern (Figure 1C) and it is plausible that selection against this pattern facilitated early animal husbandry. This study provides an interesting insight into a long-standing evolutionary question. The dramatic phenotypic differences between wild and domestic taxa could either be the result of altered selection upon pre-existing variation in the wild ancestor once under human control, or the result of selection for new mutations with major effects that arise after the domestication process has begun. The MC1R locus in pigs provides a clear example of the latter case. Specifically, the EP allele provides particularly strong evidence for this since it involves two mutations with distinct phenotypic effects: the D124N missense mutation causes dominant black color, and the two base pair insertion at codon 22 causes a frameshift that results in inactivation of the MC1R locus. The combination of these two mutations leads to a unique allele and resulting coat color, neither of which could have evolved in a wild context since the appearance of either of the two mutations would have been eliminated from the population by purifying selection. The additive nature of mutations found within domestic MC1R alleles proves that shifts in selection pressure can lead to rapid phenotypic change as newly favored alleles form the templates on which additional mutations can be added to create novel phenotypic effects. It is common knowledge that there has been selection acting on coat color phenotypes in domestic animals since color has been used as breed characteristics. However, breed formation is a very recent phenomenon (within the last few hundred years) and the possibility that coat color variants have been accumulating due to relaxed selection since domestication and then been under strong selection during breed formation has not been excluded. This study demonstrates that selection on coat color phenotypes has a much older history and must trace back to the early period of domestication. Materials and Methods Sample Location and Collection DNA samples from 68 unrelated domestic pigs (no common grandparents) were included in the study. The material comprised 45 European pigs representing 31 populations and 23 Chinese pigs representing 19 breeds. The Chinese pigs included members from each of the six traditional types of Chinese indigenous pig breeds described by Zhang [25]. In addition, three Chinese wild boars from two different regions and 12 European wild boars from Poland were included. Genomic DNA was extracted from blood by standard methods or from hair roots by Chelex extraction. Sequencing An MC1R fragment including the entire coding region plus 43 bp of 5′-UTR and 208 bp of 3′-UTR was amplified with the forward EPIG16 primer [7] and the reverse primer PCR2 (5′-CGCCGTCTCTCCAGCCTCCCCCACTC-3′). PCR was carried out on a DNA Engine Gradient Cycler (Perkin Elmer, Norwalk, Connecticut, USA) in a total volume of 35 µl containing 70 ng genomic DNA, 0.5 mM of both primers, 0.3 mM dNTPs, 1× PCR Gold Buffer, 2 U AmpliTaq Gold enzyme (Perkin Elmer, Norwalk, Connecticut, USA), 1 M Betaine (SIGMA, Missouri, USA) and 2.5 mM MgCl2. The PCR profile was 45 cycles of 45 s each at 94°C, 63.5°C and 72°C; the cycles were preceded by 7 min at 94°C and terminated with 10 min at 72°C. Three other sequencing primers (Seq1: 5′-GTCCATCTTCTACGCGCT-3′; Seq2: 5′-GGTGGTAGTAGGCGATGA-3′ and Seq3: 5′-GGT TCT TGG CGA TGG CGG –3′) were designed to produce a final 963/965 bp sequence including the entire MC1R coding region. The sequences from one sample were compiled into a single contiguous fragment using SEQUENCHER (Gene Codes, Ann Arbor, Michigan, USA). Ambiguous positions were verified by resequencing. The haplotypes carried by heterozygous animals were deduced by sequencing cloned PCR products. Heterozygosity for the Ep mutation comprising a two bp insertion was further verified by fragment analysis as previously described [7]. Phylogenetic Methods – dN/dS Calculation A network tree of the MC1R sequences was constructed by hand. The relative frequencies of non-synonymous (dN) and synonymous (dS) substitutions were calculated using the Nei-Gojobori method in MEGA4 [26],[27]. Standard errors were estimated with a bootstrap procedure (500 replicates) and the statistical significance of differences in dN and dS values was calcuated with a Z test [27],[28]. Nomenclature We propose a new more informative nomenclature for porcine MC1R alleles (Table S1). The nomenclature is composed of four digits where the first two digits are used to distinguish alleles that show documented phenotypic differences and corresponds to the five previously described alleles. The two last digits are used to distinguish alleles presumed to be associated with the same phenotype. Accession Numbers All novel sequences were submitted to GenBank with reference numbers EU443644-EU443726. Supporting Information Table S1. New and old nomenclature for porcine MC1R/Extension (E) alleles. (0.01 MB PDF) Click here for additional data file. Table S2. Sequence alignment of pig MC1R/E alleles. A dash (-) indicates identity to the master sequence. (0.04 MB PDF) Click here for additional data file. Table S3. MC1R and Extension genotypes among all tested pigs. (0.02 MB PDF) Click here for additional data file. Table S4. Extension/MC1R allele frequencies among European and Asian pigs. (0.01 MB PDF) Click here for additional data file.

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Contributors

María Muñoz: Role: Data curationRole: Formal analysisRole: Writing – original draft

Riccardo Bozzi: Role: InvestigationRole: SupervisionRole: Writing – review & editing

Fabián García: Role: MethodologyRole: ResourcesRole: Writing – review & editing

Yolanda Núñez: Role: InvestigationRole: MethodologyRole: Writing – review & editing

Claudia Geraci:

ORCID: http://orcid.org/0000-0002-4948-0725

Role: InvestigationRole: MethodologyRole: Writing – review & editing

Alessandro Crovetti: Role: MethodologyRole: Writing – review & editing

Juan García-Casco: Role: InvestigationRole: Writing – review & editing

Estefania Alves: Role: InvestigationRole: MethodologyRole: Writing – review & editing

Martin Škrlep: Role: InvestigationRole: ResourcesRole: Writing – review & editing

Rui Charneca:

ORCID: http://orcid.org/0000-0002-3597-6746

Role: ResourcesRole: Writing – review & editing

Jose M. Martins: Role: ResourcesRole: Writing – review & editing

Raquel Quintanilla: Role: ResourcesRole: Writing – review & editing

Joan Tibau: Role: ResourcesRole: Writing – review & editing

Goran Kušec: Role: ResourcesRole: Writing – review & editing

Ivona Djurkin-Kušec: Role: ResourcesRole: Writing – review & editing

Marie J. Mercat: Role: ResourcesRole: Writing – review & editing

Juliette Riquet: Role: ResourcesRole: Writing – review & editing

Jordi Estellé: Role: InvestigationRole: Writing – review & editing

Christoph Zimmer: Role: ResourcesRole: Writing – review & editing

Violeta Razmaite: Role: ResourcesRole: Writing – review & editing

Jose P. Araujo:

ORCID: http://orcid.org/0000-0002-1232-3160

Role: ResourcesRole: Writing – review & editing

Čedomir Radović: Role: ResourcesRole: Writing – review & editing

Radomir Savić: Role: ResourcesRole: Writing – review & editing

Danijel Karolyi:

ORCID: http://orcid.org/0000-0003-0409-9071

Role: ResourcesRole: Writing – review & editing

Maurizio Gallo: Role: Resources

Marjeta Čandek-Potokar: Role: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing

Luca Fontanesi: Role: ConceptualizationRole: Funding acquisitionRole: ResourcesRole: SupervisionRole: Writing – review & editing

Ana I. Fernández: Role: ConceptualizationRole: Funding acquisitionRole: Writing – review & editing

Cristina Óvilo:

ORCID: http://orcid.org/0000-0002-5738-8435

Role: ConceptualizationRole: InvestigationRole: Project administrationRole: SupervisionRole: Writing – original draft

Juan J. Loor: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 20 November 2018

Publication date Collection: 2018

Volume: 13

Issue: 11

Electronic Location Identifier: e0207475

Affiliations

[1 ] Departamento Mejora Genética Animal, INIA, Madrid, Spain

[2 ] Università degli Studi di Firenze, Firenze, Italy

[3 ] Department of Agricultural and Food Sciences, University of Bologna, Bologna, Italy

[4 ] Kmetijski inštitut Slovenije, Ljubljana, Slovenia

[5 ] Instituto de Ciências Agrárias e Ambientais Mediterrânicas (ICAAM), Universidade de Évora, Évora, Portugal

[6 ] Programa de Genética y Mejora Animal, IRTA, Barcelona, Spain

[7 ] University of Osijek, Faculty of Agrobiotechnical Sciences, Osijek, Croatia

[8 ] Institut du Porc, IFIP, Le Rheu, France

[9 ] Génétique Physiologie et Système d’Elevage, INRA, Castanet-Tolosan, France

[10 ] GABI, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France

[11 ] Bäuerliche Erzeugergemeinschaft Schwäbisch Hall, Schwäbisch Hall, Germany

[12 ] Animal Science Institute, Lithuanian University of Health Sciences, Baisogala, Lithuania

[13 ] Instituto Politecnico de Viana do Castelo, Viana do Castelo, Portugal

[14 ] Institute for Animal Husbandry-Pig Research Department, Belgrade-Zemun, Serbia

[15 ] University of Belgrade, Faculty of agriculture, Belgrade-Zemun, Serbia

[16 ] Department of animal science, Faculty of agriculture, University of Zagreb, Zagreb, Croatia

[17 ] Associazione Nazionale Allevatori Suini (ANAS), Roma, Italy

University of Illinois, UNITED STATES

Author notes

Competing Interests: The authors have declared that no competing interests exist, excepting that the corresponding author Cristina Óvilo is a PLOS ONE Editorial Board member. However, this does not alter the authors’ adherence to all the PLOS ONE policies.

* E-mail: ovilo@ 123456inia.es

Author information

Claudia Geraci http://orcid.org/0000-0002-4948-0725

Rui Charneca http://orcid.org/0000-0002-3597-6746

Jose P. Araujo http://orcid.org/0000-0002-1232-3160

Danijel Karolyi http://orcid.org/0000-0003-0409-9071

Cristina Óvilo http://orcid.org/0000-0002-5738-8435

Article

Publisher ID: PONE-D-18-14935

DOI: 10.1371/journal.pone.0207475

PMC ID: 6245784

PubMed ID: 30458028

SO-VID: 0738df45-17ae-466b-af6b-52de487b99ec

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This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 18 May 2018

Date accepted : 30 October 2018

Page count

Figures: 5, Tables: 7, Pages: 30

Funding

Funded by: European Union’s Horizon 2020 research and innovation programme

Award ID: 634476-TREASURE

Award Recipient :

ORCID: http://orcid.org/0000-0002-5738-8435

Cristina Óvilo

Funded by: Slovenian Research Agency

Award ID: P4-0133

Award Recipient : Marjeta Čandek-Potokar

Funded by: Slovenian Research Agency

Award ID: P4-0133

Award Recipient : Martin Škrlep

This study has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement no. 634476 to CO (project acronym TREASURE). The content of this paper reflects only the author’s view and the European Union Agency is not responsible for any use that may be made of the information it contains. MČP and MŠ were co-financed by Slovenian Research Agency (grant P4-0133). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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