Insectes Sociaux

, Volume 57, Issue 4, pp 371–377 | Cite as

The degree of parasitism of the bumblebee (Bombus terrestris) by cuckoo bumblebees (Bombus (Psithyrus) vestalis)

  • S. Erler
  • H. M. G. Lattorff
Research Article


Host–parasite systems are characterised by coevolutionary arms races between host and parasite. Parasites are often the driving force, as they replicate much faster than their hosts and have shorter generation times and larger population sizes, resulting in higher mutation rates per time interval. This scenario does not fit all host–parasite systems. Socially parasitic cuckoo bumblebees (Bombus (Psithyrus) vestalis) parasitise colonies of Bombus terrestris share most life history characteristics with their hosts. As they parasitise only a subset of all available colonies, their population size should be lower than that of their hosts. This might have strong negative effects on the genetic diversity of B. vestalis and their adaptability. Here, we study for the first time the population structure of a Bombus/Bombus (Psithyrus) system. Highly polymorphic DNA markers were used to reconstruct sibships from individuals collected in the wild. The analysis of the host and parasite populations revealed a rate of parasitism of about 42% (range 33–50%). The population size of B. vestalis was lower compared to their hosts, which was also reflected in low within-group genetic distance. An analysis of the reconstructed queen genotypes revealed more supersisters amongst the B. vestalis queens when compared to the B. terrestris host. The data suggest that B. vestalis females and males do not disperse over long distances. This shows a potential for local adaptation to their hosts.


Social parasite Psithyrus Bumblebees Sibship reconstruction 



We would like to thank the students of the 2008 summer course in ecology for the help with sampling and DNA analysis. Financial support was granted by the BMBF program FUGATO-Plus (FKZ: 0315126 to HMGL).

Supplementary material

40_2010_93_MOESM1_ESM.pdf (176 kb)
Supplementary material 1 (PDF 176 kb)


  1. Alford D.V. 1975. Bumblebees. Davis-Poynter, London, 352 ppGoogle Scholar
  2. Beye M., Hasselmann M., Fondrk M.K., Page R.E. and Omholt S.W. 2003. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114: 419-429Google Scholar
  3. Boomsma J.J. and Ratnieks F.L.W. 1996. Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. Lond. B 351: 947-975Google Scholar
  4. Brandt M., Foitzik S., Fischer-Blass B. and Heinze J. 2005. The coevolutionary dynamics of obligate ant social parasite systems – between prudence and antagonism. Biol. Rev. 80: 251-567Google Scholar
  5. Carvell C., Rothery P., Pywell R.F. and Heard M.S. 2008. Effects of resource availability and social parasite invasion on field colonies of Bombus terrestris. Ecol. Entomol. 33: 321-327Google Scholar
  6. Cornuet J.M. and Aries F. 1980. Number of sex alleles in a sample of honeybee colonies. Apidologie 11: 87-93Google Scholar
  7. Davies N.B., Bourke A.F.G. and Brooke M. de L. 1989. Cuckoos and parasitic ants: Interspecific brood parasitism as an evolutionary arms race. Trends Ecol. Evol. 4: 274-278Google Scholar
  8. Estoup A., Scholl A., Pouvreau A. and Solignac M. 1995. Monoandry and polyandry in bumble bees (Hymenoptera; Bombinae) as evidenced by highly variable microsatellites. Mol. Ecol. 4: 89-93Google Scholar
  9. Estoup A., Solignac M., Cornuet J.M., Goudet J. and Scholl A. 1996. Genetic differentiation of continental and island populations of Bombus terrestris (Hymenoptera: Apidae) in Europe. Mol. Ecol. 5: 19-31Google Scholar
  10. Fischer B. and Foitzik S. 2004. Local co-adaptation leading to a geographical mosaic of coevolution in a social parasite system. J. Evol. Biol. 17: 1026-1034Google Scholar
  11. Fisher R.M. 1988. Observations on the behaviours of three European cuckoo bumble bee species (Psithyrus). Insect. Soc. 35: 341-354Google Scholar
  12. Foitzik S., Achenbach A. and Brandt M. 2009. Locally adapted social parasite affects density, social structure, and life history of its ant hosts. Ecology 90: 1195-1206Google Scholar
  13. Gadau J., Gerloff C.U., Krüger N., Chan H., Schmid-Hempel P., Wille A. and Page R.E. 2001. A linkage analysis of sex determination in Bombus terrestris (L.) (Hymenoptera: Apidae). Heredity 87: 234-242Google Scholar
  14. Gibbs H.L., Sorenson M.D., Marchetti K., Brooke M. de L., Davies N.B. and Nakamura H. 2000. Genetic evidence for female host-specific races of the common cuckoo. Nature 407: 183-186Google Scholar
  15. Goudet J. 1995. FSTAT (Version 1.2): A computer program to calculate F-statistics. J. Hered. 86: 485-486Google Scholar
  16. Goulson D., Lye G.C. and Darvill B. 2008. Decline and conservation of bumble bees. Annu. Rev. Entomol. 53: 191-208Google Scholar
  17. Goulson D., Hanley M.E., Darvill B. and Ellis J.S. 2006. Biotope associations and the decline of bumblebees (Bombus spp.). J. Ins. Cons. 10: 95-103Google Scholar
  18. Goulson D., Hanley M.E., Darvill B., Ellis J.S. and Knight M.E. 2005. Causes of rarity in bumblebees. Biol. Cons. 122: 1-8Google Scholar
  19. Hamilton W.D., Axelrod R. and Tanese R. 1990. Sexual reproduction as an adaptation to resist parasites (a review). Proc. Natl Acad. Sci. USA 87: 3566-3573Google Scholar
  20. Kalinowski S.T. 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol. Ecol. Notes 5: 187-189Google Scholar
  21. Konovalov D.A., Manning C. and Henshaw M.T. 2004. KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol. Ecol. Notes 4: 779-782Google Scholar
  22. Kosior A., Celary W., Olejniczak P., Fijał J., Krol W., Solarz W. and Płonka P. 2007. The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41: 79-88Google Scholar
  23. Kover P.X. 2006. Evolutionary genetics of host–parasite interactions. In: Evolutionary Genetics (Fox C.W. and Wolf J.B., Eds), Oxford University Press: Oxford. pp 447-463Google Scholar
  24. Kraus F.B., Koeniger N., Tingek S. and Moritz R.F.A. 2005. Using drones for estimating colony number by microsatellite DNA analyses of haploid males in Apis. Apidologie 36: 223-229Google Scholar
  25. Kraus F.B., Wolf S. and Moritz R.F.A. 2009. Male flight distance and population substructure in the bumblebee Bombus terrestris. J. Anim. Ecol. 78: 247–252Google Scholar
  26. Küpper G. and Schwammberger K.H. 1995. Social parasitism in bumble bees (Hymenoptera, Apidae): observations of Psithyrus sylvestris in Bombus pratorum nests. Apidologie 26: 245-254Google Scholar
  27. Lepais O., Darvill B., O’Connor S., Osborne J.L., Sanderson R.A., Cussans J., Goffe L. and Goulson D. 2010. Estimation of bumblebee queen dispersal distances using sibship reconstruction method. Mol. Ecol. 19: 819-831Google Scholar
  28. Moritz R.F.A., Kraus F.B., Kryger P. and Crewe R.M. 2007. The size of wild honeybee populations (Apis mellifera) and its implications for the conservation of honeybees. J. Ins. Cons. 11: 391-397Google Scholar
  29. Müller C.B. and Schmid-Hempel P. 1992. Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites. Ecol. Entomol. 17: 343-353Google Scholar
  30. Nei M. 1972. Genetic distance between populations. Am. Nat. 106: 283-292Google Scholar
  31. Payne C.M., Laverty T.M. and Lachance M.A. 2003. The frequency of multiple paternity in bumble bee (Bombus) colonies based on microsatellite DNA at the B10 locus. Insect. Soc. 50: 375-378Google Scholar
  32. Payne R.B. 1977. The ecology of brood parasitism in birds. Annu. Rev. Ecol Syst. 8: 1-28Google Scholar
  33. Pelletier L. and McNeil J.N. 2003. The effect of food supplementation on reproductive success in bumblebee field colonies. Oikos 103: 688-694Google Scholar
  34. Raymond M. and Rousset F. 1995. GENEPOP (version 1.2): Population Genetics Software for Exact Tests and Ecumenicism. J. Hered. 86: 248-249Google Scholar
  35. Salathé M., Kouyos R.D. and Bonhoeffer S. 2008. The State of Affairs in the Kingdom of the Red Queen. Trends Ecol. Evol. 23: 439-445 Google Scholar
  36. Schmid-Hempel P., Schmid-Hempel R., Brunner P.C., Seeman O.D. and Allen G.R. 2007. Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck. Heredity 99: 414-422Google Scholar
  37. Schmid-Hempel P. 1998. Parasites in Social Insects. Princeton University Press, Princeton, 409 ppGoogle Scholar
  38. van Honk C., Röseler P.F., Velthuis H.H.W. and Malotaux M. 1981. The conquest of a Bombus terrestris colony by a Psithyrus vestalis female. Apidologie 12: 57-67Google Scholar
  39. Walsh P.S., Metzger D.A. and Higuchi R. 1991. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506-513Google Scholar
  40. Wang J.L. 2004. Sibship reconstruction from genetic data with typing errors. Genetics 166: 1963-1979Google Scholar
  41. Wilfert L., Gadau J. and Schmid-Hempel P. 2006. A core linkage map of the bumblebee Bombus terrestris. Genome 49: 1215-1226Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2010

Authors and Affiliations

  1. 1.Institut für Biologie, Molekulare ÖkologieMartin-Luther-Universität Halle-WittenbergHalle (Saale)Germany

Personalised recommendations