Skip to main content
Log in

Population structure of Apis cerana in Thailand reflects biogeography and current gene flow rather than Varroa mite association

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

Concordance between the mitochondrial haplotypes of the Eastern honey bee, Apis cerana, and its ectoparasitic Varroa mites across the Isthmus of Kra in Thailand has suggested that local host–pathogen co-evolution may be responsible for the geographic distribution of particular genotypes. To investigate nuclear microsatellites population structure in A. cerana, single workers of A. cerana colonies from Thailand were genotyped at 18 microsatellite loci. The loci showed intermediate to high levels of heterozygosity and a range of allele numbers. The analyses confirmed a fundamental subdivision of the Thai A. cerana population into the “Asia Mainland” and “Sundaland” regions at the Isthmus of Kra. However, the nuclear microsatellite differentiation was less distinct than mtDNA haplotype differences, suggesting male-biased dispersal and population admixture. Overall, samples showed a weak isolation-by-distance effect. The isolated population on Samui island was most differentiated from the other samples. The results do not support our initial hypothesis of local host–pathogen co-evolution, which predicts a strict correspondence between the nuclear genome and the lineage of parasitic Varroa mite of the A. cerana samples, because the gene flow indicated by our nuclear microsatellite markers should also mix potential Varroa resistance alleles among subpopulations. Instead, our study suggests that the coincidental distribution of Varroa lineages and A. cerana population structure in Thailand are the result of biogeographic history and current migration patterns.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Crozier Y.C., Koulianos S. and Crozier R.H. 1991. An improved test for Africanized honeybee mitochondrial DNA. Experientia 47: 968-969.

    Google Scholar 

  • Damus M.S. and Otis G.W. 1997. A morphometric analysis of Apis cerana F and Apis nigrocincta Smith populations from Southeast Asia. Apidologie 28: 309-323.

  • de la Rua P., Simon U.E., Tilde A.C., Moritz R.F.A. and Fuchs S. 2000. MtDNA variation in Apis cerana populations from the Philippines. Heredity 84: 124-130.

    Google Scholar 

  • Delaney D.A., Meixner M.D., Schiff N.M. and Sheppard W.S. 2009. Genetic characterization of commercial honey bee (Hymenoptera: Apidae) populations in the United States by using mitochondrial and microsatellite markers. Annls Entomol. Soc. Am. 102: 666-673.

    Google Scholar 

  • Deowanish S., Nakamura J., Matsuka M. and Kimura K. 1996. MtDNA variation among subspecies of Apis cerana using restriction fragment length polymorphism. Apidologie 27: 407-413.

    Google Scholar 

  • El-Niweiri M.A.A. and Moritz R.F.A. 2010. The impact of apiculture on the genetic structure of wild honeybee populations (Apis mellifera) in Sudan. J. Insect Cons. 14: 115-124.

    Google Scholar 

  • Evanno G., Regnaut S. and Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14: 2611-2620.

    Google Scholar 

  • Hamilton W.D. 1980. Sex versus non-sex versus parasite. Oikos 35: 282-290.

    Google Scholar 

  • Hepburn H.R., Smith D.R., Radloff S.E. and Otis G.W. 2001. Infraspecific categories of Apis cerana: morphometric, allozymal and mtDNA diversity. Apidologie 32: 3-23.

    Google Scholar 

  • Hubisz M.J., Falush D., Stephens M. and Pritchard J.K. 2009. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Res. 9: 1322-1332.

    Google Scholar 

  • Insuan S., Deowanish S., Klinbunga S., Sittipraneed S., Sylvester H.A. and Wongsiri S. 2007. Genetic differentiation of the giant honey bee (Apis dorsata) in Thailand analyzed by mitochondrial genes and microsatellites. Biochem. Gen. 45: 345-361.

    Google Scholar 

  • Lively C.M. and Dybdahl M.F. 2000. Parasite adaptation to locally common host genotypes. Nature 405: 679-681.

    Google Scholar 

  • Meznar E.R., Gadau J., Koeniger N. and Rueppell O. 2010. Comparative linkage mapping suggests a high recombination rate in all honey bees. J. Hered. 101: S118-S126.

    Google Scholar 

  • Nakamura J., Wongsiri S. and Sasaki M. 1991. Apis cerana on Samui island and its beekeeping. Honeybee Sci. 12: 27-30.

    Google Scholar 

  • Oldroyd B.P. and Wongsiri S. 2006. Asian Honey Bees: Biology, Conservation and Human Interactions. Harvard University Press, Cambridge. 360 pp.

  • Ozdil F., Yildiz M.A. and Hall H.G. 2009. Molecular characterization of Turkish honey bee populations (Apis mellifera) inferred from mitochondrial DNA RFLP and sequence results. Apidologie 40: 570-576.

    Google Scholar 

  • Palmer K.A. and Oldroyd B.P. 2000. Evolution of multiple mating in the genus Apis. Apidologie 31: 235-248.

    Google Scholar 

  • Pamilo P., Gertsch P., Thoren P. and Seppa P. 1997. Molecular population genetics of social insects. Annu. Rev. Ecol. Syst. 28: 1-25.

    Google Scholar 

  • Pritchard J.K., Stephens M. and Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.

    Google Scholar 

  • Raffiudin R. and Crozier R.H. 2007. Phylogenetic analysis of honey bee behavioral evolution. Mol. Phyl. Evol. 43: 543-552.

    Google Scholar 

  • Rosenkranz P., Aumeier P. and Ziegelmann B. 2010. Biology and control of Varroa destructor. J. Invertebr. Pathol. 103: S96-S119.

    Google Scholar 

  • Ross K.G., Krieger M.J., Shoemaker D.D., Vargo E.L. and Keller L. 1997. Hierarchical analysis of genetic structure in native fire ant populations: results from three classes of molecular markers. Genetics 147: 643-55.

    Google Scholar 

  • Rousset F. 2008. GENEPOP ‘ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Res. 8: 103-106.

    Google Scholar 

  • Ruttner F. 1988. Biogeography and Taxonomy of Honeybees. Springer, Berlin. 284 pp.

  • Sammataro D., Gerson U. and Needham G. 2000. Parasitic mites of honey bees: Life history, implications, and impact. Annu. Rev. Entomol. 45: 519-548.

    Google Scholar 

  • Schmid-Hempel P. 1998. Parasites in Social Insects. Princeton University Press, Princeton, NJ. 392 pp.

  • Schug M.D., Regulski E.E., Pearce A. and Smith S.G. 2004. Isolation and characterization of dinucleotide repeat microsatellites in Drosophila ananassae. Gen. Res. 83: 19-29.

    Google Scholar 

  • Sihanuntavong D., Sittipraneed S. and Klinbunga S. 1999. Mitochondrial DNA diversity and population structure of the honey bee, Apis cerana, in Thailand. J. Apicult. Res. 38: 211-219.

  • Sittipraneed S., Laoaroon S., Klinbunga S. and Wongsiri S. 2001a. Genetic differentiation of the honey bee (Apis cerana) in Thailand: evidence from microsatellite polymorphism. J. Apicult. Res. 40: 9-16.

  • Sittipraneed S., Sihanuntavong D. and Klinbunga S. 2001b. Genetic differentiation of the honey bee (Apis cerana) in Thailand revealed by polymorphism of a large subunit of mitochondrial ribosomal DNA. Insect. Soc. 48: 266-272.

  • Smith D.R. and Hagen R.H. 1996. The biogeography of Apis cerana as revealed by mitochondrial DNA sequence data. J. Kansas Entomol. Soc. 69: 294-310.

    Google Scholar 

  • Smith D.R. and Hagen R.H. 1999. Phylogeny and Biogeography of Apis cerana subspecies: testing alternative hypotheses. In: Apiculture for the 21st Century (Hoopingarner R. and Connor L., Eds), Wicwas Press, Cheshire, pp 60-68.

  • Smith D.R., Villafuerte L., Otis G. and Palmer M.R. 2000. Biogeography of Apis cerana F. and A. nigrocincta Smith: insights from mtDNA studies. Apidologie 31: 265-279.

    Google Scholar 

  • Solignac M., Mougel F., Vautrin D., Monnerot M. and Cornuet J.M. 2007. A third-generation microsatellite-based linkage map of the honey bee, Apis mellifera, and its comparison with the sequence-based physical map. Genome Biol. 8: R66.

    Google Scholar 

  • Songram O., Sittipraneed S. and Klinbunga S. 2006. Mitochondrial DNA diversity and genetic differentiation of the honeybee (Apis cerana) in Thailand. Biochem. Gen. 44: 256-269.

    Google Scholar 

  • Sylvester H.A., Limbipichai K., Wongsiri S., Rinderer T.E. and Mardan M. 1998. Morphometric studies of Apis cerana in Thailand and the Malaysian peninsula. J. Apicult. Res. 37: 137-145.

    Google Scholar 

  • Takahashi J.I., Shimizu S., Koyama S., Kimura K., Shimizu I. and Yoshida T. 2009. Variable microsatellite loci isolated from the Asian honeybee, Apis cerana (Hymenoptera; Apidae). Mol. Ecol. Res. 9: 819-821.

    Google Scholar 

  • Warrit N., Smith D.R. and Lekprayoon C. 2006. Genetic subpopulations of Varroa mites and their Apis cerana hosts in Thailand. Apidologie 37: 19-30.

    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. and Tsutsui N.D. 2006. Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science 314: 642-645.

    Google Scholar 

  • Woodruff D.S. 2003. Neogene marine transgressions, palaeogeography and biogeographic transitions on the Thai-Malay Peninsula. J. Biogeogr. 30: 551-567.

    Google Scholar 

Download references

Acknowledgments

We would like to thank Stephen Brown for practical assistance in the lab. Members of the UNCG social insect lab and the North Carolina Honey Bee Research Consortium improved the study through many comments and discussions. The study was further improved by constructive criticisms by three anonymous reviewers and our editor. This study was financially supported by the National Science Foundation (#0615502) and USDA-NIFA (AFRI #2010-65-104-20533).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. Rueppell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rueppell, O., Hayes, A.M., Warrit, N. et al. Population structure of Apis cerana in Thailand reflects biogeography and current gene flow rather than Varroa mite association. Insect. Soc. 58, 445–452 (2011). https://doi.org/10.1007/s00040-011-0161-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-011-0161-2

Keywords

Navigation