Abstract
The Iberian honey bee has been one of the most surveyed subspecies for genetic diversity. Yet, previous studies have missed an important component of Iberian honey bee variation harbored by populations inhabiting the Atlantic side of the Iberian Peninsula. Herein, we provide a fuller picture of the Iberian honey bee maternal diversity by revealing 16 novel haplotypes detected in honey bees from Portugal. Of the 16 haplotypes, all of African ancestry, 15 belong to the Atlantic sub-lineage AIII while only one fits the most common sub-lineage AI. This level of new variation is remarkable as it represents a 59% increase in the wide-range African lineage and a 188% in sub-lineage AIII. Our findings further highlight the complexity of the Iberian honey bee diversity patterns and reinforce the importance of this southernmost European territory as a reservoir of Apis mellifera genetic diversity, a resource increasingly important in a rapidly changing and demanding world.
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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
Bandelt, H.J., Forster, P., Rohl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48
Cánovas, F., De la Rúa, P., Serrano, J., Galián, J. (2008) Geographical patterns of mitochondrial DNA variation in Apis mellifera iberiensis (Hymenoptera: Apidae). J. Zool. Syst. Evol. Res. 46, 24–30
Cánovas, F., De la Rúa, P., Serrano, J., Galián, J. (2011) Microsatellite variability reveals beekeeping influences on Iberian honeybee populations. Apidologie. 42, 235–251
Collet, T., Ferreira, K.M., Arias, M.C., Soares, A.E.E., Del Lama, M.A. (2006) Genetic structure of Africanized honeybee populations (Apis mellifera L.) from Brazil and Uruguay viewed through mitochondrial DNA COI–COII patterns. Heredity. 97, 329–335
Cornuet, J.M., Fresnaye, J. (1989) Biometrical study of honey bee populations from Spain and Portugal. Apidologie. 20, 93–101
Cornuet, J.M., Garnery, L., Solignac, M. (1991) Putative origin and function of the intergenic region between COI and COII of Apis mellifera L. mitochondrial DNA. Genetics. 128, 393–403
Crozier, R.H., Crozier, Y.C. (1993) The mitochondrial genome of the honey bee Apis mellifera: complete sequence and genome organization. Genetics. 133, 97–117
De la Rúa, P., Serrano, J., Galián, J. (1998) Mitochondrial DNA variability in the Canary islands honeybees (Apis mellifera L.). Mol. Ecol. 7, 1543–1547
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
De la Rúa, P., Galián, J., Serrano, J., Moritz, R.F.A. (2002) Microsatellite analysis of non-migratory colonies of Apis mellifera iberica from south-eastern Spain. J. Zool. Syst. Evol. Research. 40, 164–168
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, 339–350
De la Rúa, P., Jiménez, Y., Galián, J., Serrano, J. (2004) Evaluation of the biodiversity of honey bee (Apis mellifera) populations from eastern Spain. J. Apic. Res. 43, 162–166
De la Rúa, P., Hernandez-Garcia, R., Jiménez, Y., Galián, J., Serrano, J. (2005) Biodiversity of Apis mellifera iberica (Hymenoptera: Apidae) from northeastern Spain assessed by mitochondrial analysis. Insect Syst. Evol. 36, 21–28
De la Rúa, P., Galián, J., Pedersen, B.V., Serrano, J. (2006) Molecular characterization and population structure of Apis mellifera from Madeira and the Azores. Apidologie. 37, 699–708
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
Dietemann, V., Pirk, C.W.W., Crewe, R. (2009) Is there a need for conservation of honeybees in Africa?. Apidologie. 40, 285–295
Engel, M.S. (1999) The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis). J. Hym. Res. 8, 165–196
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
Franck, P., Garnery, L., Loiseau, A., Oldroyd, B.P., Hepburn, H.R., Solignac, M., Cornuet, J.M. (2001) Genetic diversity of the honey bee in Africa: microsatellite and mitochondrial data. Heredity. 86, 420–430
Garnery, L., Solignac, M., Celebrano, G., Cornuet, J.M. (1993) A simple test using restricted PCR-amplified mitochondrial DNA to study the genetic structure of Apis mellifera L. Experientia. 49, 1016–1021
Garnery, L., Mosshine, E.H., Oldroyd, B.P., Cornuet, J.M. (1995) Mitochondrial DNA variation in Moroccan and Spanish honey bee populations. Mol. Ecol. 4, 465–471
Garnery, L., Franck, P., Baudry, E., Vautrin, D., Cornuet, J.M., Solignac, M. (1998a) Genetic diversity of the west European honey bee (Apis mellifera mellifera and A. m. iberica). I. Mitochondrial DNA. Genet. Sel. Evol. 30, S31-S47
Garnery, L., Franck, P., Baudry, E., Vautrin, D., Cornuet, J.M., Solignac, M. (1998b) Genetic diversity of the west European honey bee (Apis mellifera mellifera and A. m. iberica). II. Microsatellite loci. Genet. Sel. Evol. 30, S49-S74
Gómez, A., Lunt, D.H. (2007). Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. Springer, Dordrecht
Haddad, N., Meixner, M.D., Fuchs, S., Migdadi, H., Garnery, L., Sheppard, W.S. (2009) Mitochondrial DNA support for genetic reserves of Apis mellifera syriaca in Jordan. J. Apic. Res. 48, 19–22
Hewitt, G.M. (1999) Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68, 87–112
Hewitt, G.M. (2001) Speciation, hybrid zones and phylogeography—or seeing genes in space and time. Mol. Ecol. 10, 537–549
Jensen, A.B., Palmer, K.A., Boomsma, J.J., Pedersen, B.V. (2005) 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
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
Miguel, I., Baylac, M., Iriondo, M., Manzano, C., Garnery, L., Estonba, A. (2010) Both geometric morphometric and microsatellite data consistently support the differentiation of the Apis mellifera M evolutionary branch. Apidologie. 42, 150–161
Prada, Q.C.F., Duran, J.T., Salamanca, G.G., Del Lama, M.A. (2009) Population genetics of Apis mellifera L. (Hymenoptera: Apidae) from Columbia. J. Apic. Res. 48, 3–10
Rortais, A., Arnold, G., Alburaki, M., Legout, H., Garnery, L. (2011) Review of the DraI COI–COII test for the conservation of the black honeybee (Apis mellifera mellifera). Conserv. Genet. Resour. 3, 383–391
Ruttner, F., Tassencourt, L., Louveaux, J. (1978) Biometrical–statistical analysis of the geographic variability of Apis mellifera L. Apidologie. 9, 363–381
Sheppard, W.S., Meixner, M.D. (2003) Apis mellifera pomonella, a new honey bee subspecies from Central Asia. Apidologie. 34, 367–375
Smith, D.R., Glenn, T.C. (1995) Allozyme polymorphisms in spanish honeybees (Apis mellifera iberica). J. Hered. 86, 12–16
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
Szalanski, A.L., Magnus, R.M. (2010) Mitochondrial DNA characterization of Africanized honey bee (Apis mellifera L.) populations from the USA. J. Apic. Res. 49, 177–185
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol. Biol. Evol. doi:10.1093/molbev/msr121
Acknowledgments
We are indebted to numerous technicians of the Divisões de Intervenção Veterinária (Direcção Geral de Veterinária) and of the Beekeeping Associations, who kindly provided the honey bee samples. Financial support was provided by Fundação para a Ciência e Tecnologia and COMPETE/QREN/EU (project PTDC/BIA-BEC/099640/2008), Programa Apícola Nacional (Medida 6A) to M. A. Pinto, and by Fundación Séneca (project 11961/PI/09) to P. De la Rúa. We also thank the two anonymous reviewers for their valuable comments.
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La façade atlantique de la péninsule ibérienne : un « point chaud » pour une nouvelle diversité maternelle de type africain chez l’abeille
Abeille ibérienne / diversité génétique / ADN mitochondrial / test Dra I / Portugal
Die atlantische Seite der iberischen Halbinsel: ein Hotspot für bisher unbekannte Afrika-typische maternale Diversität bei Honigbienen
Iberische Honigbiene / genetische Diversität / mtDNA / DraI-Test / Portugal
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Pinto, M.A., Muñoz, I., Chávez-Galarza, J. et al. The Atlantic side of the Iberian Peninsula: a hot-spot of novel African honey bee maternal diversity. Apidologie 43, 663–673 (2012). https://doi.org/10.1007/s13592-012-0141-1
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DOI: https://doi.org/10.1007/s13592-012-0141-1