Distribution of honey bee mitochondrial DNA haplotypes in an Italian region where a legislative act is protecting the Apis mellifera ligustica subspecies.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
04 Sep 2024
Historique:
received: 27 04 2024
accepted: 26 08 2024
medline: 5 9 2024
pubmed: 5 9 2024
entrez: 4 9 2024
Statut: epublish

Résumé

The conservation of the genetic integrity of Apis mellifera subspecies has emerged as an important objective. In 2019, the Emilia-Romagna region became the first Italian regional authority to issue a law specifically addressing the protection of the native Apis mellifera ligustica subspecies. In this study we analysed a highly informative portion of the mitochondrial DNA (mtDNA), widely used for assessing genetic diversity of honey bee populations. By analysing 1143 honey bees sampled after the introduction of this law, we provided a snapshot of the distribution of mtDNA haplotypes in this region. The two most frequent mtDNA haplotypes were C1 (characteristic of A. m. ligustica) and C2 (characteristic of A. m. carnica), reported in 86.5% and 11.0% of the analysed bees, respectively. About 1.3% and 1.1% of the analysed bees carried mtDNA haplotypes of the A and M lineages (haplotypes A1a, A1e, A4, A26, A65 and two novel ones, A2w and A6a; M3, M3a, M4 and M79). Continued genetic monitoring will be important to assess the impact of this regional law over the coming years. Based on the obtained results, we recommend a more stringent policy to prevent the erosion of the genetic integrity of the native subspecies A. m. ligustica.

Identifiants

pubmed: 39232026
doi: 10.1038/s41598-024-71233-5
pii: 10.1038/s41598-024-71233-5
doi:

Substances chimiques

DNA, Mitochondrial 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

20583

Subventions

Organisme : Fulbright Association
ID : Fulbright - Italy 2022-23
Organisme : Università di Bologna
ID : 2020-2021 RFO
Organisme : Regione Emilia-Romagna
ID : BEE-RER-3 projects - CUP E37G22000030007 - del Regolamento (UE) no. 1308/2013 - (OCM Apicoltura)

Informations de copyright

© 2024. The Author(s).

Références

Ruttner, F. Morphometric Analysis and Classification in Biogeography and Taxonomy of Honeybees (Springer, 1988).
Bouga, M. et al. A review of methods for discrimination of honey bee populations as applied to European beekeeping. J. Apic. Res. 50, 51–84 (2011).
doi: 10.3896/IBRA.1.50.1.06
Meixner, M. D. et al. Standard methods for characterising subspecies and ecotypes of Apis mellifera. J. Apic. Res. 52, 1–28 (2013).
doi: 10.3896/IBRA.1.52.4.05
Ilyasov, R. A., Lee, M., Takahashi, J., Kwon, H. W. & Nikolenko, A. G. A revision of subspecies structure of western honey bee Apis mellifera. Saudi J. Biol. Sci. 27, 3615–3621 (2020).
pubmed: 33304172 pmcid: 7714978 doi: 10.1016/j.sjbs.2020.08.001
De la Rúa, P., Jaffé, R., Dall’Olio, R., Muñoz, I. & Serrano, J. 2009 Biodiversity, conservation and current threats to European honeybees. Apidologie 40, 263–284 (2009).
Meixner, M. D. et al. Conserving diversity and vitality for honey bee breeding. J. Apic. Res. 49, 85–92 (2010).
doi: 10.3896/IBRA.1.49.1.12
Requier, F. et al. The conservation of native honey bees is crucial. Trends Ecol. Evol. 34, 789–798 (2019).
pubmed: 31072605 doi: 10.1016/j.tree.2019.04.008
Garnery, L., Cornuet, J. M. & Solignac, M. Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Mol. Ecol. 1, 145–154 (1992).
pubmed: 1364272 doi: 10.1111/j.1365-294X.1992.tb00170.x
Wallberg, A. et al. A worldwide survey of genome sequence variation provides insight into the evolutionary history of the honeybee Apis mellifera. Nat. Genet. 46, 1081–1088 (2014).
pubmed: 25151355 doi: 10.1038/ng.3077
Arias, M. C. & Sheppard, W. S. Molecular phylogenetics of honey bee subspecies (Apis mellifera L.) inferred from mitochondrial DNA sequence. Mol. Phylogenet. Evol. 5, 557–566 (1996).
pubmed: 8744768 doi: 10.1006/mpev.1996.0050
Alburaki, M., Moulin, S., Legout, H., Alburaki, A. & Garnery, L. Mitochondrial structure of Eastern honeybee populations from Syria Lebanon and Iraq. Apidologie 42, 628–641 (2011).
doi: 10.1007/s13592-011-0062-4
Franck, P. et al. Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data. Heredity 86, 420–430 (2001).
pubmed: 11520342 doi: 10.1046/j.1365-2540.2001.00842.x
Whitfield, C. W. et al. Thrice out of Africa: Ancient and recent expansions of the honey bee Apis mellifera. Science 314, 642–645 (2006).
pubmed: 17068261 doi: 10.1126/science.1132772
Cridland, J. M., Tsutsui, N. D. & Ramírez, S. R. The complex demographic history and evolutionary origin of the Western honey bee Apis mellifera. Genome Biol. Evol. 9, 457–472 (2017).
pubmed: 28164223 pmcid: 5381634 doi: 10.1093/gbe/evx009
Oleksa, A., Kusza, S. & Tofilski, A. Mitochondrial DNA suggests the introduction of honeybees of African ancestry to East-Central Europe. Insects 12, 410 (2021).
pubmed: 34063321 pmcid: 8147603 doi: 10.3390/insects12050410
Nazzi, F. Morphometric analysis of honey bees from an area of racial hybridization in northeastern Italy. Apidologie 23, 89–96 (1992).
doi: 10.1051/apido:19920201
Cornuet, J. M., Garnery, L. & Solignac, M. Putative origin and function of the intergenic region between COI and COII of Apis mellifera L. mitochondrial DNA. Genetics 128, 393–403 (1991).
pubmed: 1649072 pmcid: 1204476 doi: 10.1093/genetics/128.2.393
Garnery, L., Solignac, M., Celebrano, G. & Cornuet, J. M. A simple test using restricted PCR-amplified mitochondrial DNA to study the genetic structure of Apis mellifera L. Experientia 49, 1016–1021 (1993).
doi: 10.1007/BF02125651
Rortais, A., Arnold, G., Alburaki, M., Legout, H. & Garnery, L. Review of the DraICOI-COII test for the conservation of the black honeybee (Apis mellifera mellifera). Conserv. Genet. Resour. 3, 383–391 (2011).
doi: 10.1007/s12686-010-9351-x
Chávez-Galarza, J. et al. Mitochondrial DNA variation of Apis mellifera iberiensis: further insights from a large-scale study using sequence data of the tRNAleu-cox2 intergenic region. Apidologie 48, 533–544 (2017).
doi: 10.1007/s13592-017-0498-2
Chávez-Galarza, J. et al. Mitochondrial DNA variation in Peruvian honey bee (Apis mellifera L) populations using the tRNAleu-cox2 intergenic region. Insects 12, 641 (2021).
pubmed: 34357301 pmcid: 8303314 doi: 10.3390/insects12070641
Alburaki, M. et al. Honey bee populations of the USA display restrictions in their mtDNA haplotype diversity. Front. Genet. 13, 1092121 (2023).
pubmed: 36685818 pmcid: 9845583 doi: 10.3389/fgene.2022.1092121
Kaskinova, M. D., Salikhova, A. M., Gaifullina, L. R. & Saltykova, E. S. Genetic methods in honey bee breeding. Vavilov J. Genet. Breed. 27, 366 (2023).
doi: 10.18699/VJGB-23-44
Fontana, P. et al. Appeal for biodiversity protection of native honey bee subspecies of Apis mellifera in Italy (San Michele all’Adige declaration). Bull. Insectol. 71, 257–271 (2018).
Franck, P., Garnery, L., Celebrano, G., Solignac, M. & Cornuet, J. M. Hybrid origins of honey bees from Italy (Apis mellifera ligustica) and Sicily (A. m. sicula). Mol. Ecol. 9, 907–921 (2000).
pubmed: 10886654 doi: 10.1046/j.1365-294x.2000.00945.x
Oleksa, A., Chybicki, I., Tofilski, A. & Burczyk, J. Nuclear and mitochondrial patterns of introgression into native dark bees (Apis mellifera mellifera) in Poland. J. Apic. Res. 50, 116–129 (2011).
doi: 10.3896/IBRA.1.50.2.03
Jensen, A. B., Palmer, K. A., Boomsma, J. J. & Pedersen, B. V. Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Mol. Ecol. 14, 93–106 (2005).
pubmed: 15643954 doi: 10.1111/j.1365-294X.2004.02399.x
Strange, J. P., Garnery, L. & Sheppard, W. S. Morphological and molecular characterization of the Landes honey bee (Apis mellifera L.) ecotype for genetic conservation. J. Insect Conserv. 12, 527–537 (2008).
doi: 10.1007/s10841-007-9093-6
Muñoz, I. & la Rúa, P. D. Temporal analysis of the genetic diversity in a honey bee mating area of an island population (La Palma, Canary Islands, Spain). J. Apic. Sci. 56, 41–49 (2012).
Pinto, M. A. et al. Genetic integrity of the Dark European honey bee (Apis mellifera mellifera) from protected populations: a genome-wide assessment using SNPs and mtDNA sequence data. J. Apic. Res. 53, 269–278 (2014).
doi: 10.3896/IBRA.1.53.2.08
Ellis, J. S. et al. Introgression in native populations of Apis mellifera mellifera L: implications for conservation. J. Insect Conserv. 22, 377–390 (2018).
doi: 10.1007/s10841-018-0067-7
Hassett, J. et al. A significant pure population of the dark European honey bee (Apis mellifera mellifera) remains in Ireland. J. Apic. Res. 57, 337–350 (2018).
doi: 10.1080/00218839.2018.1433949
Muñoz, I. & De La Rúa, P. Wide genetic diversity in Old World honey bees threaten by introgression. Apidologie 52, 200–217 (2021).
doi: 10.1007/s13592-020-00810-0
Tanasković, M. et al. MtDNA analysis indicates human-induced temporal changes of Serbian honey bees diversity. Insects 12, 767 (2021).
pubmed: 34564207 pmcid: 8472511 doi: 10.3390/insects12090767
Yanbaev, Y. et al. Spatial analysis of genetic variation in a natural population of the dark forest bee (Apis mellifera mellifera L.) from the Southern Urals (Russia). Int. J. Environ. Studies 81, 1441–1454 (2024).
doi: 10.1080/00207233.2022.2058768
Conte, Y. L. & Navajas, M. Climate change: impact on honey bee populations and diseases. Rev. Sci. Tech. Off. Int. Epiz. 27, 499–510 (2008).
vanEngelsdorp, D. & Meixner, M. D. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J. Invertebr. Pathol. 103, S80–S95 (2010).
pubmed: 19909973 doi: 10.1016/j.jip.2009.06.011
Potts, S. G. et al. Declines of managed honey bees and beekeepers in Europe. J. Apic. Res. 49, 15–22 (2010).
doi: 10.3896/IBRA.1.49.1.02
Chauzat, M. P. et al. Demographics of the European apicultural industry. PLoS One 8, e79018 (2013).
pubmed: 24236084 pmcid: 3827320 doi: 10.1371/journal.pone.0079018
Flores, J. M. et al. Effect of the climate change on honey bee colonies in a temperate Mediterranean zone assessed through remote hive weight monitoring system in conjunction with exhaustive colonies assessment. Sci. Total Environ. 653, 1111–1119 (2019).
pubmed: 30759551 doi: 10.1016/j.scitotenv.2018.11.004
Nielsdatter, M. G., Larsen, M., Nielsen, L. G., Nielsen, M. M. & Rasmussen, C. History of the displacement of the European dark bee (Apis mellifera mellifera) in Denmark. J. Apic. Res. 60, 13–18 (2021).
doi: 10.1080/00218839.2020.1826111
Vercelli, M., Novelli, S., Ferrazzi, P., Lentini, G. & Ferracini, C. A qualitative analysis of beekeepers’ perceptions and farm management adaptations to the impact of climate change on honey bees. Insects 12, 228 (2021).
pubmed: 33800740 pmcid: 7998300 doi: 10.3390/insects12030228
Panziera, D., Requier, F., Chantawannakul, P., Pirk, C. W. W. & Blacquière, T. The diversity decline in wild and managed honey bee populations urges for an integrated conservation approach. Front. Ecol. Evol. 10, 767950 (2022).
doi: 10.3389/fevo.2022.767950
Vecchi, A. Sulla distribuzione geografica dell’Apis mellifica ligustica Spin. Italia. Bollettino del Laboratorio di Zoologia Generale e Agraria Della R. Scuola Superiore d’Agricoltura in Portici 20, 150–168 (1927).
Techer, M. A. et al. Large-scale mitochondrial DNA analysis of native honey bee Apis mellifera populations reveals a new African subgroup private to the South West Indian Ocean islands. BMC Genet. 18, 53 (2017).
pubmed: 28577537 pmcid: 5457595 doi: 10.1186/s12863-017-0520-8
Sinacori, A., Rinderer, T. E., Lancaster, V. & Sheppard, W. S. A morphological and mitochondrial assessment of Apis mellifera from Palermo Italy. Apidologie 29, 481–490 (1998).
doi: 10.1051/apido:19980601
Muñoz, I., Dall’Olio, R., Lodesani, M. & De La Rúa, P. 2009 Population genetic structure of coastal Croatian honeybees (Apis mellifera carnica). Apidologie 40, 617–626 (2009).
Utzeri, V. J., Ribani, A., Taurisano, V. & Fontanesi, L. Entomological authentication of honey based on a DNA method that distinguishes Apis mellifera mitochondrial C mitotypes: Application to honey produced by A. m ligustica and A. m carnica. Food Control. 134, 108713 (2022).
doi: 10.1016/j.foodcont.2021.108713
Fontanesi, L., Taurisano, V., Ribani, A. & Utzeri, V. J. A reply to the Letter to the Editor of Moškrič et al. entitled “A comment on the paper from Utzeri et al. (2022) “Entomological authentication of honey based on a DNA method that distinguishes Apis mellifera mitochondrial C mitotypes: Application to honey produced by A. m. ligustica and A. m. carnica, Food control, Volume 121, March 2021, 107626”. Food Control 147, 109570, (2023).
Utzeri, V. J., Ribani, A., Taurisano, V., Banqué, C. H. I. & Fontanesi, L. Distribution of the main Apis mellifera mitochondrial DNA lineages in Italy assessed using an environmental DNA approach. Insects 12, 620 (2021).
pubmed: 34357280 pmcid: 8304627 doi: 10.3390/insects12070620
Regione Emilia-Romagna. Legge regionale 4 Marzo 2019, n. 2. Norme per lo sviluppo, l'esercizio e la tutela dell'apicoltura in Emilia-Romagna. https://demetra.regione.emilia-romagna.it/al/monitor.php?urn=er:assemblealegislativa:legge:2019;2 (2019).
Dimech, D. C., Borg, S., Buttigieg, A. J. & Farrugia, D. Review of the Maltese and European Laws related to the Genetic Protection of the Endemic Maltese Honey Bee (Apis mellifera ruttneri). Eur. Energy Envtl. L. Rev. 32, 145–154 (2023).
doi: 10.54648/EELR2023007
Tamura, K., Stecher, G. & Kumar, S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 38, 3022–3027 (2021).
pubmed: 33892491 pmcid: 8233496 doi: 10.1093/molbev/msab120
Nei, M. & Tajima, F. Genetic drift and estimation of effective population size. Genetics 98, 625–640 (1981).
pubmed: 17249104 pmcid: 1214463 doi: 10.1093/genetics/98.3.625
Sušnik, S., Kozmus, P., Poklukar, J. & Meglic, V. Molecular characterisation of indigenous Apis mellifera carnica in Slovenia. Apidologie 35, 623–636 (2004).
doi: 10.1051/apido:2004061
Stevanovic, J., Stanimirovic, Z., Radakovic, M. & Kovacevic, S. R. Biogeographic study of the honey bee (Apis mellifera L.) from Serbia, Bosnia and Herzegovina and Republic of Macedonia Based on mitochondrial DNA analyses. Russ. J. Genet. 46, 603–609 (2010).
doi: 10.1134/S1022795410050145
Collet, T., Ferreira, K. M., Arias, M. C., Soares, A. E. E. & Del Lama, M. A. Genetic structure of Africanized honeybee populations (Apis mellifera L.) from Brazil and Uruguay viewed through mitochondrial DNA COI–COII patterns. Heredity 97, 329–335 (2006).
pubmed: 16955114 doi: 10.1038/sj.hdy.6800875
Magnus, R. & Szalanski, A. L. Genetic evidence for honey bees (Apis mellifera L.) of Middle Eastern lineage in the United States. Sociobiology 55, 285 (2010).
Munoz, I., Stevanović, J., Stanimirović, Z. & De la Rua, P. Genetic variation of Apis mellifera from Serbia inferred from mitochondrial analysis. J. Apic. Sci. 56, 59–69 (2012).
Magnus, R. M., Tripodi, A. D. & Szalanski, A. L. Mitochondrial DNA diversity of honey bees (Apis mellifera) from unmanaged colonies and swarms in the United States. Biochem. Genet. 52, 245–257 (2014).
pubmed: 24526322 doi: 10.1007/s10528-014-9644-y
Ostroverkhova, N. V. et al. Genetic diversity of the locus COI-COII of mitochondrial DNA in honeybee populations (Apis mellifera L.) from the Tomsk region. Russ. J. Genet. 51, 80–90 (2015).
doi: 10.1134/S102279541501010X
Szalanski, A. L., Tripodi, A. D., Trammel, C. E. & Downey, D. Mitochondrial DNA genetic diversity of honey bees, Apis mellifera Hawaii. Apidologie 47, 679–687 (2016).
doi: 10.1007/s13592-015-0416-4
Muñoz, I. & De la Rúa, P. Wide genetic diversity in Old World honey bees threaten by introgression. Apidologie 52, 200–217 (2020).
doi: 10.1007/s13592-020-00810-0
Porrini, L. P. et al. Current genetic diversity of managed and commercially produced Apis mellifera colonies in Argentina inferred by wing geometric morphometrics and COI-COII mtDNA locus. Apidologie 53, 61 (2022).
doi: 10.1007/s13592-022-00970-1
Kaskinova, M. D., Gaifullina, L. R. & Saltykova, E. S. Haplotypes of the tRNAleu-COII mtDNA region in Russian Apis mellifera populations. Animals 13, 2394 (2023).
pubmed: 37508171 pmcid: 10376158 doi: 10.3390/ani13142394
Orlovskytė, S., Budrys, E., Skrodenytė-Arbačiauskienė, V. & Blažytė-Čereškienė, L. The dark European honey bee Apis mellifera mellifera in Lithuania: data on mitotype diversity of native bee population. J. Apic. Res. 1–4 (2024).
Tanasković, M. et al. Further evidence of population admixture in the Serbian honey bee population. Insects 13, 180 (2022).
pubmed: 35206752 pmcid: 8879341 doi: 10.3390/insects13020180
Bertrand, B. et al. Mt DNA COI-COII marker and drone congregation area: An efficient method to establish and monitor honeybee (Apis mellifera L.) conservation centres. Mol. Ecol. Res. 15, 673–683 (2015).
doi: 10.1111/1755-0998.12339
Smith, D. R. et al. Geographical overlap of two mitochondrial genomes in Spanish honeybees (Apis mellifera iberica). J. Hered. 82, 96–100 (1991).
pubmed: 2013694 doi: 10.1093/oxfordjournals.jhered.a111062
Miguel, I., Iriondo, M., Garnery, L., Sheppard, W. S. & Estonba, A. Gene flow within the M evolutionary lineage of Apis mellifera: Role of the Pyrenees, isolation by distance and post-glacial recolonization routes in the western Europe. Apidologie 38, 141–155 (2007).
doi: 10.1051/apido:2007007
Garnery, L., Mosshine, E. H., Oldroyd, B. P. & Cornuet, J. M. Mitochondrial DNA variation in Moroccan and Spanish honey bee populations. Mol. Ecol. 4, 465–472 (1995).
doi: 10.1111/j.1365-294X.1995.tb00240.x
Cánovas, F., De la Rúa, P., Serrano, J., Galián, J. & De la Rúa, P. Geographical patterns of mitochondrial DNA variation in Apis mellifera iberiensis (Hymenoptera: Apidae). J. Zool. Syst. Evol. Res. 46, 24–30 (2007).
Pinto, M. A. et al. Maternal diversity patterns of Ibero-Atlantic populations reveal further complexity of Iberian honeybees. Apidologie 44, 430–439 (2013).
doi: 10.1007/s13592-013-0192-y
Abrahamovich, A. H., Atela, O., De la Rúa, P. & Galián, J. Assessment of the mitochondrial origin of honey bees from Argentina. J. Apic. Res. 46, 191–194 (2007).
doi: 10.1080/00218839.2007.11101391
Branchiccela, B. et al. Genetic changes in Apis mellifera after 40 years of Africanization. Apidologie 45, 752–756 (2014).
doi: 10.1007/s13592-014-0293-2
Agra, M. N. et al. Molecular characterization of Apis mellifera colonies from Argentina: Genotypic admixture associated with ecoclimatic regions and apicultural activities. Entomol. Exp. Appl. 166, 724–738 (2018).
doi: 10.1111/eea.12719
Tibatá, V. M. et al. Determination of the Africanized mitotypes in populations of honey bees (Apis mellifera L.) of Colombia. J. Apic. Res. 57, 219–227 (2018).
doi: 10.1080/00218839.2017.1409065
Düttmann, C. et al. Africanized honeybee population (Apis mellifera L) in Nicaragua: Forewing length and mitotype lineages. PLoS One 17, e0267600 (2022).
pubmed: 35468163 pmcid: 9037913 doi: 10.1371/journal.pone.0267600
Lin, W., McBroome, J., Rehman, M. & Johnson, B. R. Africanized bees extend their distribution in California. PLoS One 13, e0190604 (2018).
pubmed: 29346390 pmcid: 5773081 doi: 10.1371/journal.pone.0190604
Schumacher, M. J. Significance of Africanized bees for public health: a review. Arch. Int. Med. 155, 2038–2043 (1995).
doi: 10.1001/archinte.1995.00430190022003
Bovo, S. et al. A genotyping by sequencing approach can disclose Apis mellifera population genomic information contained in honey environmental DNA. Sci. Rep. 12, 19541 (2022).
pubmed: 36379985 pmcid: 9666642 doi: 10.1038/s41598-022-24101-z

Auteurs

Valeria Taurisano (V)

Animal and Food Genomics Group, Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy.

Anisa Ribani (A)

Animal and Food Genomics Group, Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy.

Dalal Sami (D)

Animal and Food Genomics Group, Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy.

Kate Elise Nelson Johnson (KE)

Animal and Food Genomics Group, Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy.

Giuseppina Schiavo (G)

Animal and Food Genomics Group, Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy.

Valerio Joe Utzeri (VJ)

Animal and Food Genomics Group, Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy.

Samuele Bovo (S)

Animal and Food Genomics Group, Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy.

Luca Fontanesi (L)

Animal and Food Genomics Group, Division of Animal Sciences, Department of Agricultural and Food Sciences, University of Bologna, Viale Giuseppe Fanin 46, 40127, Bologna, Italy. luca.fontanesi@unibo.it.

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