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Microsatellite variability reveals beekeeping influences on Iberian honeybee populations

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Abstract

The genetic structure of the Iberian honey bee (Apis mellifera iberiensis) was studied by analysing 10 microsatellite loci in 362 workers representative of nine Spanish provinces. Heterozygosity values of Iberian honeybee populations are intermediate between African and west European ones whereas allelic diversity is remarkably high at several loci. There is no definite geographic structure of Iberian honeybee populations. At a peninsular scale, the expected clinal pattern observed with mitochondrial data has been probably lost due to the extensive practice of mobile beekeeping and increased colony trade-off. Due to these practices, it is expected that the genetic homogenisation will increase during the next years. Though this might have positive effects on honey production, putative ecotypes existing in Iberia would be prone to disappear.

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References

  • Arias, M.C., Sheppard, W.S. (1996) Molecular phylogenetics of honeybee subspecies (Apis mellifera L.) inferred from mitochondrial DNA sequences. Mol. Phylogenet. Evol. 5, 557–566

    Article  PubMed  CAS  Google Scholar 

  • Arias, M.C., Rinderer, T.E., Sheppard, W.S. (2006) Further characterization of honey bees from the Iberian Peninsula by allozyme, morphometric and mtDNA haplotype analyses. J. Apic. Res. 45, 188–196

    Article  CAS  Google Scholar 

  • Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., Bonhomme, F. (2004) GENETIX, version: 4.05.2: logiciel sous WindowsTM pour la génétique des populations. Laboratoire Génome, Populations, Interactions. Université de Monftpellier II. Available from: http://www.genetix.univ-montp2.fr/genetix/genetix.htm

  • Cánovas, F., De la Rúa, P., Serrano, J., Galián, J. (2008) Geographic patterns of mitochondrial DNA variation in Apis mellifera iberiensis (Hymenoptera: Apidae). J. Zool. Syst. Evol. Res. 46, 24–30

    Google Scholar 

  • Cavalli-Sforza, L.L., Edwards, A.W.F. (1967) Phylogenetic analysis: models and estimation procedures. Evolution 32, 550–570

    Article  Google Scholar 

  • Chapuis, M.P., Estoup, A. (2007) Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24, 621–631

    Article  PubMed  CAS  Google Scholar 

  • De la Rúa, P., Galián, J., Serrano, J., Moritz, R.F.A. (2001) Molecular characterization and population structure of the honeybees from the Balearic Islands (Spain). Apidologie 32, 417–427

    Article  Google Scholar 

  • De la Rúa, P., Serrano, J., Galián, J. (2002a) Biodiversity of Apis mellifera populations from Tenerife (Canary Islands) and hybridisation with East European races. Biod. Cons. 11, 59–67

    Article  Google Scholar 

  • De la Rúa, P., Serrano, J., Galián, J. (2002b) Biodiversity of Apis mellifera populations from Tenerife (Canary Islands) and hybridisation with East European races. Biod. Cons. 11, 59–67

    Google Scholar 

  • De la Rúa, P., Galián, J., Serrano J., Moritz R.F.A. (2002b) Microsatellite analysis of non-migratory colonies of Apis mellifera iberica from south-eastern Spain. J. Zool. Syst. Evol. Res. 40, 164–168

    Article  Google Scholar 

  • De la Rúa, P., Galián, J., Serrano, J., Moritz, R.F.A. (2003) Genetic structure of Balearic honeybee populations based on microsatellite polymorphism, Genet. Sel. Evol. 35, 1–12

    Google Scholar 

  • De la Rúa, P., Jiménez, Y., Galián, J., Serrano, J. (2004a) Evaluation of the biodiversity of honey bee (Apis mellifera) populations from eastern Spain. J. Apic. Res. 43, 162–166

    Google Scholar 

  • De la Rúa, P., Hernández-García, R., Pedersen, B.V., Galián, J., Serrano, J. (2004b) Molecular diversity of honeybee Apis mellifera iberica L (Hymenoptera: Apidae) from western Andalusia. Arch. Zootec. 53, 195–203

    Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing v2.8.1. Available from: http://www.r-project.org.

  • GRASS Development Team (2008) Geographic resources analysis support system (GRASS) v6.3.0. Available from: http://grass.osgeo.org

  • Epperson, B., Li, T. (1996) Measurement of genetic structure within populations using Moran's spatial autocorrelation statistics. Proc. Natl. Acad. Sci. USA 93, 10528–10532

    Article  PubMed  CAS  Google Scholar 

  • Estoup, A., Garnery, L., Solignac, M., Cornuet, J.M. (1995) Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140, 679–695

    PubMed  CAS  Google Scholar 

  • Franck, P., Garnery, L., Solignac, M., Cornuet, J.M. (1998) The origin of West European subspecies of honeybees (Apis mellifera): new insights from microsatellite and mitochondrial data. Evolution 52, 1119–1134

    Article  CAS  Google Scholar 

  • Franck, P., Garnery, L., Loiseau, A., Hepburn, H.R., Solignac, M., Cornuet, J.M. (2001) Genetic diversity of the honeybee in Africa: microsatellite and mitochondrial data. Heredity 86, 420–430

    Article  PubMed  CAS  Google Scholar 

  • Garnery, L., Cornuet, J.M., Solignac, M. (1992) Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Mol. Ecol. 1, 145–154

    Article  PubMed  CAS  Google Scholar 

  • Garnery, L., Frank, P., Baudry, E., Vautrin, D., Cornuet, J.M., Solignac, M. (1998a) Genetic diversity of the west European honeybee (Apis mellifera mellifera and A. m. iberica). I. Mitochondrial DNA. Genet. Sel. Evol. 30, 31–47

    Article  Google Scholar 

  • Garnery, L., Frank, P., Baudry, E., Vautrin, D., Cornuet, J.M., Solignac, M. (1998b) Genetic diversity of the west European honeybee (Apis mellifera mellifera and A. m. iberica). II. Microsatellite loci. Genet. Sel. Evol. 30, 49–74

    Article  Google Scholar 

  • Gómez-Pajuelo, A. (1988) Situation of the varroatosis in Spain and Portugal. Present status of varroatosis in Europe and progress in the Varroa mite control, in: Cavalloro, R. (ed.) Proceedings of the Meeting of EC Experts’ Group Udine, Italy, pp. 41–43. ommission of the European Communities, Luxembourg

    Google Scholar 

  • Gómez-Pajuelo, A. (2003) Introducción de reinas en las colmenas, Vida Apícola117

  • Hanotte, O., Bradle, D.G., Ochieng, J.W., Verjee., Y, Hill, E.W., Rege, E.O. (2002) African pastoralism: genetic imprints of origins and migrations. Science 296, 336–339

    Article  PubMed  CAS  Google Scholar 

  • Kraus, F.B. (2005) Requirements for local population conservation and breeding. In: Lodesani, M., Costa, C. (eds.) Beekeeping and conserving biodiversity of honeybees. Sustainable bee breeding, theoretical and practical guide, pp. 87–107. Northern Bee Books, Hebden Bridge

    Google Scholar 

  • Kumar, J., Nelson, R.J., Zeigler, R.S. (1999) Population structure and dynamics of Magnaporthe grisea in the Indian Himalayas. Genetics 152, 971–984

    PubMed  CAS  Google Scholar 

  • Manel, S., Schwartz, M.K., Luikart, G., Tarberlet, P. (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol. Evol. 18, 189–197

    Article  Google Scholar 

  • Manni, F., Guérard, E., Heyer, E. (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by “Monmonier’s algorithm”. Hum. Biol. 76, 173–190

    Article  PubMed  Google Scholar 

  • Mantel, N. (1967) The detection of disease clustering and a generalised regression approach. Cancer Res. 27, 209–220

    PubMed  CAS  Google Scholar 

  • Mattila, H.R., Seeley, T.D. (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317, 362–364

    Article  PubMed  CAS  Google Scholar 

  • Miguel, I., Iriondo, M., Garnery, L., Sheppard, W.S., Estonba, A. (2007) Gene flow within the M evolutionary lineage of Apis mellifera: role of the Pyrenees, isolation by distance and post-glacial re-colonization routes in the western Europe. Apidologie 38, 141–155

    Article  CAS  Google Scholar 

  • Nei, M. (1978) Estimation of average heterozigosity and genetic distance from a small number of individuals. Genetics 89, 583–590

    PubMed  CAS  Google Scholar 

  • Pereira, T.C., Bittencourt, V.D.A., Secolin, R., de Souza-Rocha, C., de Godoy- Maia, C., Lopes-Cendes, I. (2007) Strand analysis, a free online program for the computational identification of the best RNA interference (RNAi) targets based on Gibbs free energy. Genet. Mol. Biol. 30, 1206–1208

    Article  CAS  Google Scholar 

  • Perrier, C., Strange, J., Langella, O., Sheppard, W.S., Garnery, L. (2003) Diversité génétique, introgressions mitochondriales et nucléaires dans une population d'abeilles des Landes de Gascogne. Actes du Bureau de Recherches Génétiques 4, 79–100

    Google Scholar 

  • Pritchard, J., Stephens, M., Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959

    PubMed  CAS  Google Scholar 

  • Raymond, M., Rousset, F. (1995a) An exact test for population differentiation. Evolution 49, 1280–1283

    Article  Google Scholar 

  • Raymond, M., Rousset, F. (1995b) GENEPOP version 1.2: a population genetics software for exact test and ecumenicism. J. Hered. 86, 248–249

    Google Scholar 

  • Ruíz, M., Ruíz, J.P. (1986) Ecological history of trashumance in Spain. Biol. Conserv. 37, 73–86

    Article  Google Scholar 

  • Ruttner, F. (1988) Biogeography and taxonomy of honeybees. Springer-Verlag, Berlin

    Google Scholar 

  • Slatkin, M. (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47, 264–279

    Article  Google Scholar 

  • Smith, D.R., Palopoli, M.F., Taylor, B.R., Garnery, L., Cornuet, J.M., Solignac, M., Brown, W.M. (1991) Geographical overlap of two mitochondrial genomes in Spanish honeybees (Apis mellifera iberica). J. Hered. 82, 96–100

    PubMed  CAS  Google Scholar 

  • Smouse, P.E., Peakall, R. (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82, 561–573

    Article  PubMed  Google Scholar 

  • Solignac, M., Vautrin, D., Loiseau, A., Mougel, F., Baudry, E., Estoup, A., Garnery, L., Haberl, M., Cornuet, J.M. (2003) Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Mol. Ecol. Notes 3, 307–311

    Article  CAS  Google Scholar 

  • Streiff, R., Labbe, T., Bacilieri, R., Steinkellner, H., Glossl, J., Krener, A. (1998) Within-population genetic structure in Quercus robur L. and Quercus petraea (Matt.) Liebl. assessed with isozymes and microsatellites. Mol. Ecol. 7, 317–328

    Article  Google Scholar 

  • Walsh, P.S., Metzger, D.A., Higuchi, R. (1991) ChelexR 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506–513

    PubMed  CAS  Google Scholar 

  • Whitfield, C.W., Behura, S.K., Berlocher, S.H., Clark, A.G., Johnston, J.S., Sheppard, W.S., Smith, D.R., Suarez, A.V., Weaver, D., Tsutsui, N.D. (2006) Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 314, 642–645

    Article  PubMed  CAS  Google Scholar 

  • Wright, S. (1951) The genetical structure of populations. Ann. Eugen. 15, 323–354

    Article  Google Scholar 

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Acknowledgements

Thanks are due to the many beekeepers and associations who generously collaborated with us in collecting the samples. Special thanks to O Rodríguez, J Ornia, E Muñiz, U Mediel and COAG association. Thanks to Dr. O Langella for his support with Populations software. We thank three anonymous referees for their valuable suggestions. This research has been supported by projects RZ00-013 (Instituto Nacional de Investigaciones Agrarias, INIA, Spain), EVK2 2000–00628 (European 5th Framework), BOS2003-9765 (Ministerio de Educación y Ciencia, Spain) and API06-010 COORD-2 (Ministerio de Agricultura, Pesca y Alimentación, Spain).

La variabilité des microsatellites révèle les effets de l’apiculture sur les populations d’abeilles espagnoles.

Apis mellifera / génétique des populations / cartes synthétiques

Zusammenfassung – Die Variabilität von Mikrosatelliten zeigt den Einfluss der Imkerei auf Populationen der Honigbiene in Spanien. Es ist bisher nicht klar, ob der bei den Bienen Iberiens beobachtete, den Breitengraden folgende Gradient der mitochondrialen DNA auch bei Mikrosatellitenmarkern auftritt. Erste Ergebnisse dazu zeigten eine höhere Variabilität von Mikrosatelliten in Afrika gegenüber Iberien und Frankreich, als Folge eines vermuteten genetischen Flaschenhalses während der letzten Eiszeit. Neuere Ergebnisse zeigten jedoch eine vergleichbar große Diversität in Populationen aus Belgien, Frankreich und Iberien. Es wurde vermutet, dass diese Ähnlichkeit durch die höheren Mutationsraten der Mikrosatelliten verursacht wurde, die die genetischen Effekte der Wiederbesiedlung nach der letzten Eiszeit verdeckt haben könnten.

Die zu testende Ausgangshypothese besagt, dass iberische Honigbienenpopulationen eine abnehmende Diversität von Süden nach Norden zeigen, wobei die Unterschiede zwischen Populationen hauptsächlich durch einen Isolation-by-Distance-Effekt zu erklären wären. Dazu wurden 10 Mikrosatellitenmarker in neun Populationen der Iberischen Halbinsel untersucht.

Der ausgeprägte Grad an genetischer Homogenität lässt vermuten, dass in jüngster Zeit ein beträchtlicher Genfluss zwischen den verschiedenen iberischen Populationen stattgefunden hat. Zwei verschiedene Prozesse können dafür verantwortlich sein. Der eine hängt damit zusammen, dass durch Varroa verlorenen gegangene Bienenvölkern wieder aufgebaut werden mussten. Dazu wurden verstärkt Ableger oder Schwärme gebildet, sowie Völker (oder begattete Königinnen), oft aus entfernten Gegenden, zusätzlich gekauft. Der andere Einfluss ist die Wanderimkerei, die im Durchschnitt 28.58% der spanischen Bienenstände betrifft (von 94.86% in Valencia bis 0.98% in Galizien, einschließlich La Coruña, Pontevedra und Orense).

Aus den Ergebnissen schließen wir, dass die Honigbienen von Iberien eine nahezu homogene Population bilden, jedoch mit einer Differenzierung zwischen einer östlichen, mediterranen Subpopulation (repräsentiert von Tarragona und Valencia), und einer westlichen, die die anderen Gebiete der Halbinsel einschließt.

Dieser unerwartete Grad an Homogenisierung wird wahrscheinlich durch Handel mit Völkern zwischen entfernten Gegenden und durch Wanderimkerei verursacht – das Ausmaß dieser Einflüsse muss jedoch noch bestimmt werden. Der Gesamteffekt dieser Prozesse liegt in einer Zunahme der genetischen Diversität innerhalb der Völker, zur Steigerung der Fitness und der Produktivität. Jedoch wird diese Homogenisierung zum Verlust möglicherweise vorhandener Ökotypen beitragen, das heißt, von Populationen, die an spezifische lokale Bedingungen nach vielen Generationen natürlicher und imkerlicher Selektion gut angepasst sind. In den nächsten Jahren wird es eine wichtige Aufgaben sein, Beiträge zur Erhaltung dieser Ökotypen zu leisten.

Apis mellifera / Populationsgenetik / Synthesekarten

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Authors and Affiliations

  1. Área de Biología Animal, Dpto. de Zoología y Antropología Física, Facultad de Veterinaria; Campus de Espinardo, 30100, Murcia, Spain

    Fernando Cánovas, Pilar de la Rúa, José Serrano & José Galián

  2. Marine Ecology and Evolution Team; Centro de Ciências do Mar (CCMAR, CIMAR-Laboratório Associado), Universidade do Algarve; Campus de Gambelas, 8005–139, Faro, Portugal

    Fernando Cánovas

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  1. Fernando Cánovas
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  2. Pilar de la Rúa
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  3. José Serrano
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  4. José Galián
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Correspondence to Fernando Cánovas.

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Manuscript editor: Marina Meixner

Appendices

Appendix I

  Sampling descriptions.
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Appendix II

  Allelic frequencies, observed heterozygosity (H o ) and gene diversity (H e ) of nine honeybee populations of A. m. iberiensis.
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Cánovas, F., de la Rúa, P., Serrano, J. et al. Microsatellite variability reveals beekeeping influences on Iberian honeybee populations. Apidologie 42, 235–251 (2011). https://doi.org/10.1007/s13592-011-0020-1

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