Skip to main content
Log in

The Atlantic side of the Iberian Peninsula: a hot-spot of novel African honey bee maternal diversity

  • Original article
  • Published:
Apidologie Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1.
Figure 2.
Figure 3.
Figure 4.

Similar content being viewed by others

References

  • 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 

  • Bandelt, H.J., Forster, P., Rohl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37–48

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Cánovas, F., De la Rúa, P., Serrano, J., Galián, J. (2011) Microsatellite variability reveals beekeeping influences on Iberian honeybee populations. Apidologie. 42, 235–251

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cornuet, J.M., Fresnaye, J. (1989) Biometrical study of honey bee populations from Spain and Portugal. Apidologie. 20, 93–101

    Article  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  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., 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

    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, 339–350

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dietemann, V., Pirk, C.W.W., Crewe, R. (2009) Is there a need for conservation of honeybees in Africa?. Apidologie. 40, 285–295

    Article  Google Scholar 

  • Engel, M.S. (1999) The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis). J. Hym. Res. 8, 165–196

    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., 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gómez, A., Lunt, D.H. (2007). Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. Springer, Dordrecht

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Hewitt, G.M. (1999) Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. 68, 87–112

    Article  Google Scholar 

  • Hewitt, G.M. (2001) Speciation, hybrid zones and phylogeography—or seeing genes in space and time. Mol. Ecol. 10, 537–549

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  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 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ruttner, F., Tassencourt, L., Louveaux, J. (1978) Biometrical–statistical analysis of the geographic variability of Apis mellifera L. Apidologie. 9, 363–381

    Article  Google Scholar 

  • Sheppard, W.S., Meixner, M.D. (2003) Apis mellifera pomonella, a new honey bee subspecies from Central Asia. Apidologie. 34, 367–375

    Article  Google Scholar 

  • Smith, D.R., Glenn, T.C. (1995) Allozyme polymorphisms in spanish honeybees (Apis mellifera iberica). J. Hered. 86, 12–16

    PubMed  CAS  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 

  • 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

    Article  CAS  Google Scholar 

  • 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

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Alice Pinto.

Additional information

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

Manuscript editor: Marina Meixner

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13592-012-0141-1

Keywords

Navigation