The origin of west European subspecies of honeybees (Apis mellifera): New insights from microsatellite and mitochondrial data

Evolution

Volumn 52, Issue 4, 1998, Pages 1119-1134

  Franck, Pierre ^a   Garnery, Lionel ^b   Solignac, Michel ^a   Cornuet, Jean Marie ^a  

^a CNRS   (France)

^b CEMAGREF   (France)

Author keywords

Apis mellifera; Intergradation; Microsatellite; MtDNA; Population genetics; SSR

Indexed keywords

EVOLUTION; GENETICS; HONEYBEE; MITOCHONDRIAL DNA;

APIDAE; APIS MELLIFERA; HYMENOPTERA;

EID: 0031668826     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1558-5646.1998.tb01839.x     Document Type: Article

References (49)

1. ALPATOV, W. W. 1929. Biometrical studies on variation and races of honeybee. Q. Rev. Biol. 4:1-58.
2. AUBERT, J., AND M. SOLIGNAC. 1990. Experimental evidence for mitochondrial DNA intogression between Drosophila species. Evolution 44:1272-1282.
3. BALLARD, J. W. O., AND M. KREITMAN. 1995. Is mitochondrial DNA a strictly neutral marker? Trends Ecol. Evol. 10:485-488.
4. CAVALLI-SFORZA, L. L., AND A. W. F. EDWARDS. 1967. Phylogenetic analysis: models and estimation procedures. Am. J. Hum. Genet. 19:233-257.
5. CHAKRABORTY, R., AND L. JIN. 1993. A unified approach to study hypervariable polymorphisms: statistical considerations of determining relatedness and population distance. Pp. 153-175 in S. D. J. Pena, R. Chakraborty, J. T. Epplen, and A. J. Jeffreys, eds. DNA fingerprinting: state of the science. Birkhauser Verlag Basel, Switzerland.
6. CORNUET, J.-M. 1982. The MDH polymorphism in some west mediterranean honeybee populations. IUSSI congress, Boulder, CO.
7. _. 1983. Reproduction, génétique et sélection de l'abeille. Bull. Tech. Apic. 10:13-36.
8. CORNUET, J.-M., AND J. FRESNAYE. 1989. Etude biométrique de colonies d'abeilles d'Espagne et du Portugal. Apidologie 20:91-101.
9. CORNUET, J.-M., AND L. GARNERY. 1991. Mitochondrial DNA variability in honeybees and its phylogeographic implications. Apidologie 22:627-642.
10. CORNUET, J.-M., AND G. LUIKART. 1996. Description and power analysis of two tests for inferring recent population bottlenecks from allele frequency data. Genetics 144:2001-2014.
11. CORNUET, J.-M., J. FRESNAYE, AND L. TASSENCOURT. 1975. Discrimination et classification de populations d'abeilles à partir de caractères biométriques. Apidologie 6:145-187.
12. CORNUET, J.-M., J. FRESNAYE, AND P. LAVIE. 1978. Etude biométrique de deux populations d'abeilles cévenoles. Apidologie 9:41-55.
13. CORNUET, J.-M., J. ALBISETTI, N. MALLET, AND J. FRESNAYE. 1982. Etude biométrique d'une population d'abeilles landaises. Apidologie 13:3-13.
14. CORNUET, J.-M., A. DOUADI, H. MOSSHINE, AND J. FRESNAYE. 1988. Etude biométrique de populations d'abeilles marocaines. Apidologie 19:355-366.
15. CORNUET, J.-M., L. GARNERY, AND M. SOLIGNAC. 1991. Putative origin and function of the COI-COII intergenic region of Apis mellifera L. mitochondrial DNA. Genetics 1128:393-403.
16. CORNUET, J.-M., B. P. OLDROYD, AND R. H. CROZIER. 1995, Unequal thermostability of allelic forms of malate dehydrogenase in honeybees. J. Apic. Res. 34:45-47.
17. CRANDALL, K. A., AND A. R. TEMPLETON. 1993. Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny recontruction. Genetics 134:959-969.
18. ESTOUP, A., L. GARNERY, M. SOLIGNAC, AND J.-M. CORNUET. 1995a. 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.
19. ESTOUP, A., C. TAILLIEZ, J.-M. CORNUET, AND M. SOLIGNAC. 1995b. Size homoplasy and mutational processes of interrupted micro- satellites in apidae species, Apis mellifera and Bombus terrestris. Mol. Biol. Evol. 12:1074-1084.
20. FELSENSTEIN, J. 1993. PHYLIP: phylogeny inference package. Vers. 3.5. University of Washington, Seattle, WA.
21. GARNERY, L., AND J.-M. CORNUET. 1994. Inter and intra lineage mitochondrial DNA variation in the honeybee Apis mellifera. 12th IUSSI Congress, Paris.
22. GARNERY, L., D. VAUTRIN, J.-M. CORNUET, M. SOLIGNAC. 1991. Phylogenic relationships in the genus Apis inferred from mitochondrial DNA sequence data. Apidologie 22:87-92.
23. GARNERY, L., J.-M. CORNUET, AND M. SOLIGNAC. 1992. Evolutionary history of the honey bee Apis mellifera inferred from mitochondrial DNA analysis. Mol. Ecol. 1:145-154.
24. GARNERY, L., M. SOLIGNAC, G. CELEBRANO, AND J.-M. CORNUET. 1993. A simple test using restricted PCR-amplified mitochondrial DNA to study the genetic structure of Apis mellifera. Experientia 49:1016-1021.
25. GARNERY, L., H. MOSSHINE, B. P. OLDROYD, AND J.-M. CORNUET. 1995. Mitochondrial DNA variation in Moroccan and Spanish honey bee populations. Mol. Ecol. 4:465-471.
26. GYAPAI, G., J. MORISSETTE, A. VIGNAL, C. DIB, C. FIZAMES, P. MILLASSEAU, S. MARC, G. BERNARDI, M. LATHROP, AND J. WEISSENBACH. 1994. The 1993-94 Généthon human genetic linkage map. Nat. Genet. 7:246-339.
27. HALL, H. G., AND D. R. SMITH. 1991. Distinguishing African and European honeybee matrilines using amplified mitochondrial DNA. Proc. Nat. Acad. Sci. USA 88:4548-4552.
28. HEDGES, S. B. 1992. The number of replications needed for accurate estimation of the bootstrap P value in phylogenetic studies. Mol. Biol. Evol. 9:366-369.
29. HEPBURN, H. R., AND S. E. RADLOFF. 1996. Morphometric and pheromonal analyses of Apis mellifera L. along a transect from Sahara to the Pyrenees. Apidologie 27:35-45.
30. KOCHER, T. D., W. K. THOMAS, A. MEYER, S. V. EDWARDS, F. X. VILLABLANCA, A. C. WILSON. 1989. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Nat. Acad. Sci. USA 86:6196-6200.
31. NEI, M. 1978. Estimation of average heterozygoty and genetic distance from a small number of individuals. Genetics 89:145-163.
32. NEI, M., AND F. TAJIMA. 1981. DNA polymorphism detectable by restriction endonucleases. Genetics 97:583-590.
33. OLDROYD, B. P., D. ROWE, J.-M. CORNUET, T. E. RINDERER, AND R. H. CROZIER. 1994. Racial admixture of Apis mellifera in Tasmania, Australia: similarities and differences with natural hybrid zones in Europe. Heredity 74:315-325.
34. ORANTES-BERMEJO, F. J., AND P. GARCIA-FERNANDEZ. 1995. Morphological variability of Apis mellifera iberica in different apiaries of southern Spain. J. Apic. Res. 34:13-30.
35. RAYMOND, M., AND F. ROUSSET. 1995. Genepop (version 1.2): population genetics software for exact test and ecumenism. J. Hered. 86:248-250.
36. RUBINSZTEIN, D. C., W. AMOS, J. LEGGO, S. GOODBURN, S. JAIN, S. H. LI, R. L. MARGOLIS, C. A. Ross, AND M. A. FERGUSSONSMITH. 1995. Microsatellite evolution: evidence for directionality and variation in rate between species. Nat. Genet. 10:337-343.
37. RUTTNER, F. 1988. Biogeography and taxonomy of honeybees. Springer-Verlag, Berlin.
38. RUTTNER, F., L. TASSENCOURT, AND J. LOUVEAUX. 1978. Biometrical-statistical analysis of the geographic variability of Apis mellifera L. Apidologie 9:363-381.
39. SAITOU, N., AND M. NEI. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
40. SHEPPARD, W. S., T. E. RINDERER, J. A. MAZZOLI, J. A. STELZER, AND H. SHIMANUKI. 1991. Gene flow between African and European-derived honeybee populations in Argentina. Nature. 349:782-784.
41. SLATKIN, M. 1993. Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47:264-279.
42. SMITH, D. R. 1991. African bees in Americas: insight from biogeography and genetic. Trends Ecol. Evol. 6:17-21.
43. SMITH, D. R., AND T. C. GLENN. 1995. Allozyme polymorphisms in Spanish honeybees (Apis mellifera iberica). J. Hered. 86:1216.
44. SMITH, D. R., M. F. PALOPOLI, B. R. TAYLOR, L. GARNERY, J.-M. CORNUET, M. SOLIGNAC, AND W. M. BROWN. 1991. Geographical overlap of two mitochondrial genomes in Spanish honeybees (Apis mellifera iberica). J. Hered. 82:96-100.
45. SNEDECOR, G. W., AND W. G. COCHRAN. 1978. Statistical methods. Iowa State Univ. Press, Ames, IA.
46. SWOFFORD, D. L. 1989. PAUP: phylogenetic analysis using parsimony. Rel. 3. Illinois Natural History Survey, Champaign, IL.
47. TAKEZAKI, N., AND M. NEI. 1996. Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144:389-399.
48. WATTERSON, G. A., AND H. A. GUESS. 1977. Is the most frequent allele the oldest, Theor. Popul. Biol. 11:141-160.
49. WEBER, J. L., AND C. WRONG. 1993. Mutation of human short tandem repeats. Hum. Mol. Genet. 2:1123-1128.