Microsatellite variability reveals beekeeping influences on Iberian honeybee populations

Apidologie

Volumn 42, Issue 3, 2011, Pages 235-251

  Cánovas, Fernando ^a,b   De La Rúa, Pilar ^a   Serrano, José ^a   Galián, José ^a  

^a Facultad de Veterinaria   (Spain)

^b UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

Apis mellifera; Population genetics; Synthesis maps

Indexed keywords

AGRICULTURAL PRODUCTION; ALLELE; APICULTURE; ECOTYPE; GENETIC MARKER; GENETIC STRUCTURE; GEOGRAPHICAL VARIATION; HETEROZYGOSITY; HOMOGENEITY; HONEYBEE; MITOCHONDRIAL DNA;

IBERIAN PENINSULA; SPAIN;

APIS MELLIFERA; APIS MELLIFERA IBERICA; APIS MELLIFERA IBERIENSIS;

EID: 80054690907     PISSN: 00448435     EISSN: 12979678     Source Type: Journal    
DOI: 10.1007/s13592-011-0020-1     Document Type: Article

References (48)

1. 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 (Pubitemid 126320901)
2. 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 (Pubitemid 46086013)
3. Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., Bonhomme, F. (2004) GENETIX, version: 4.05.2: logiciel sous WindowsTM pour la géné tique des populations. Laboratoire Génome, Populations, Interactions. Université de Monftpellier II. Available from: http://www.genetix.univ- montp2.fr/genetix/genetix.htm
4. 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
5. Cavalli-Sforza, L. L., Edwards, A. W. F. (1967) Phylogenetic analysis: models and estimation procedures. Evolution 32, 550-570
6. Chapuis, M. P., Estoup, A. (2007) Microsatellite null alleles and estimation of population differentiation. Mol. Biol. Evol. 24, 621-631 (Pubitemid 46355787)
7. 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 (Pubitemid 32973213)
8. 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 (Pubitemid 34209273)
9. 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 (Pubitemid 34209273)
10. De la Rúa, P., Galián, J., Serrano J., Moritz R. F. A. (2002b) Microsatellite analysis of non-migratory colonies of Apis mellifera iberica from southeastern Spain. J. Zool. Syst. Evol. Res. 40, 164-168
11. 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
12. 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 (Pubitemid 40346394)
13. 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
14. R Development Core Team (2008) R: A language and environment for statistical computing v2.8.1. Available from: http://www.r-project.org.
15. GRASS Development Team (2008) Geographic resources analysis support system (GRASS) v6.3.0. Available from: http://grass.osgeo.org
16. 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 (Pubitemid 26314658)
17. 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
18. 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 (Pubitemid 28417892)
19. 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 (Pubitemid 32745303)
20. 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
21. 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
22. 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
23. 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
24. Gómez-Pajuelo, A. (2003) Introducción de reinas en las colmenas, Vida Apícola 117
25. 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 (Pubitemid 34303686)
26. 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
27. Kumar, J., Nelson, R. J., Zeigler, R. S. (1999) Population structure and dynamics of Magnaporthe grisea in the Indian Himalayas. Genetics 152, 971-984 (Pubitemid 29330898)
28. Manel, S., Schwartz, M. K., Luikart, G., Tarberlet, P. (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol. Evol. 18, 189-197 (Pubitemid 36345738)
29. 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 (Pubitemid 39014211)
30. Mantel, N. (1967) The detection of disease clustering and a generalised regression approach. Cancer Res. 27, 209-220
31. Mattila, H. R., Seeley, T. D. (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317, 362-364 (Pubitemid 47106374)
32. 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 recolonization routes in the western Europe. Apidologie 38, 141-155 (Pubitemid 47173215)
33. Nei, M. (1978) Estimation of average heterozigosity and genetic distance from a small number of individuals. Genetics 89, 583-590 (Pubitemid 8396073)
34. 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
35. 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
36. Pritchard, J., Stephens, M., Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945-959 (Pubitemid 30397141)
37. Raymond, M., Rousset, F. (1995a) An exact test for population differentiation. Evolution 49, 1280-1283 (Pubitemid 3025486)
38. Raymond, M., Rousset, F. (1995b) GENEPOP version 1.2: a population genetics software for exact test and ecumenicism. J. Hered. 86, 248-249
39. Ruíz, M., Ruíz, J. P. (1986) Ecological history of trashumance in Spain. Biol. Conserv. 37, 73-86
40. Ruttner, F. (1988) Biogeography and taxonomy of honeybees. Springer-Verlag, Berlin
41. Slatkin, M. (1993) Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47, 264-279
42. 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
43. Smouse, P. E., Peakall, R. (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82, 561-573 (Pubitemid 29285226)
44. 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 (Pubitemid 36720177)
45. 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
46. 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
47. 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 (Pubitemid 44646386)
48. Wright, S. (1951) The genetical structure of populations. Ann. Eugen. 15, 323-354