Behavioral Ecology and Sociobiology

, Volume 61, Issue 10, pp 1509–1514 | Cite as

Preservation and loss of the honey bee (Apis) egg-marking signal across evolutionary time

  • Piyamas Nanork
  • Siriwat Wongsiri
  • Benjamin P. Oldroyd
Original Paper


Honey bee workers are able to distinguish queen-laid eggs from worker-laid eggs, and remove (‘police’) worker-laid eggs. The cue that police workers use is as yet unidentified but is likely to be a chemical signal. This signal benefits queens for it ensures their reproductive monopoly. It also benefits collective workers because it allows them to raise more closely related queen-laid males than the less-related sons of half sisters. Because both parties benefit from the egg-marking signal, it should be stable over evolutionary time. We show that Apis mellifera workers can distinguish queen-laid from worker-laid eggs of the dwarf honey bee A. florea, a phylogenetically distant species that diverged from the A. mellifera lineage 6–10 mya. However, A. mellifera workers are unable to distinguish worker-laid eggs of A. cerana, a much more recent divergence (2–3 mya). The apparent change in the egg-marking signal used by A. cerana may be associated with the high rates of ovary activation in this species.


Worker policing Apis florea Apis cerana Apis mellifera Signals 



This work was supported by the Thailand Research Fund and the Australian Research Council. We acknowledge the technical assistance of Asst. Prof. Dr. Sureerat Deowanish and members of the Centre of Excellence in Entomology: Bee Biology, Biodiversity of Insects and Mites, Chulalongkorn University, Bangkok, Thailand. Tom Wenseleers, Madeleine Beekman, and Bill Hughes provided thoughtful comments on earlier drafts.


  1. Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera:Apinae:Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol 37:25–35PubMedCrossRefGoogle Scholar
  2. Bai ARK, Reddy CC (1975) Ovary development and egg laying in Apis cerana indica workers. J Apic Res 14:149–152Google Scholar
  3. Barron AB, Oldroyd BP, Ratnieks FLW (2001) Worker reproduction in honey-bees (Apis) and the anarchic syndrome: a review. Behav Ecol Sociobiol 50:199–208CrossRefGoogle Scholar
  4. Beekman M (2004) Is her majesty is at home? Trends Ecol Evol 19:505–506PubMedCrossRefGoogle Scholar
  5. Beekman M, Oldroyd BP (2003) Different policing rates of eggs laid by queenright and queenless anarchistic honey-bee workers. Behav Ecol Sociobiol 54:480–485CrossRefGoogle Scholar
  6. Beekman M, Oldroyd BP (2005) Honey bee workers use cues other than egg viability for policing. Biol Lett 1:129–132PubMedCrossRefGoogle Scholar
  7. Beekman M, Martin CG, Oldroyd BP (2004) Similar policing rates of eggs laid by virgin and mated honey-bee queens. Naturwissenschaften 91:598–601PubMedCrossRefGoogle Scholar
  8. Châline N, Ratnieks FLW, Bourke T (2002) Anarchy in the UK: Detailed genetic analysis of worker reproduction in a naturally-occurring British anarchistic honeybee, Apis mellifera, colony using DNA microsatellites. Mol Ecol 11:1795–1803PubMedCrossRefGoogle Scholar
  9. Collett D (1994) Modelling survival data in medical research. Chapman & Hall, LondonGoogle Scholar
  10. D’Ettore P, Heinze J, Ratnieks FLW (2004) Worker policing by egg eating in the ponerine ant, Pachycondyla inversa. Proc R Soc Lond B 271:1427–1434CrossRefGoogle Scholar
  11. D’Ettorre P, Tofilski A, Heinze J, Ratnieks FLW (2006) Non-transferable signals on ant queen eggs. Naturwissenschaften 93:136–140PubMedCrossRefGoogle Scholar
  12. Endler A, Liebig J, Schmitt T, Parker JE, Jones GR, Schreier P, Hölldobler B (2004) Surface hydrocarbons of queen eggs regulated worker reproduction in a social insect. Proc Natl Acad Sci USA 101:2945–2950PubMedCrossRefGoogle Scholar
  13. Endler A, Liebig J, Holldobler B (2006) Queen fertility, egg marking and colony size in the ant Camponotus floridanus. Behav Ecol Sociobiol 59:490–499CrossRefGoogle Scholar
  14. Engel MS (1998) Fossil honey bees and evolution in the genus Apis (Hymenoptera: Apidae). Apidologie 29:265–281Google Scholar
  15. Engel MS (1999) The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis). J Hymenopt Res 8:165–196Google Scholar
  16. Engel MS, Schultz TR (1997) Phylogeny and behavior in honey bees (Hymenoptera: Apidae). Ann Entomol Soc Am 90:43–53Google Scholar
  17. Foster KR, Gulliver J, Ratnieks FLW (2002) Worker policing in the European hornet Vespa crabo. Insectes Soc 49:41–44CrossRefGoogle Scholar
  18. Halling LA, Oldroyd BP (2003) Do policing honeybee workers target eggs in drone comb? Insectes Soc 50:59–61CrossRefGoogle Scholar
  19. Halling LA, Oldroyd BP, Wattanachaiyingcharoen W, Barron AB, Nanork P, Wongsiri S (2001) Worker policing in the bee Apis florea. Behav Ecol Sociobiol 49:509–513CrossRefGoogle Scholar
  20. Hammond RL, Keller L (2004) Conflict over male parentage in social insects. PLoS Biol 2:1472–1482CrossRefGoogle Scholar
  21. Helanterä H, Sundström L (2005) Worker reproduction in the ant Formica fusca. J Evol Biol 18:162–171PubMedCrossRefGoogle Scholar
  22. Johnson CA, Topoff H, van der Meer RK, Lavine B (2005) Do these eggs smell funny to you?: an experimental study of egg discrimination by hosts of the social parasite Polyergus breviceps (Hymenoptera: Formicidae). Behav Ecol Sociobiol 57:245–255CrossRefGoogle Scholar
  23. Katzav-Gozansky T, Soroker V, Hefetz A (1997) Plasticity of caste-specific Dufour’s gland secretion in the honey bee (Apis mellifera L.). Naturwissenshaften 84:238–241CrossRefGoogle Scholar
  24. Katzav-Gozansky T, Soroker V, Ibarra F, Francke W, Hefetz A (2001) Dufour’s gland secretion of the queen honeybee (Apis mellifera): an egg discriminator pheromone or a queen signal? Behav Ecol Sociobiol 51:76–86CrossRefGoogle Scholar
  25. Katzav-Gozansky T, Soroker V, Hefetz A (2002) Honeybees Dufour’s gland-idiosyncrasy of a new queen signal. Apidologie 33:525–537CrossRefGoogle Scholar
  26. Katzav-Gozansky T, Soroker V, Francke W, Hefetz A (2003a) Honeybee egg-laying workers mimic a queen signal. Insectes Soc 50:20–23CrossRefGoogle Scholar
  27. Katzav-Gozansky T, Soroker V, Kamer J, Schulz C, Franke W, Hefetz A (2003b) Ultrastructural and chemical characterization of egg surface of honeybee worker and queen-laid eggs. Chemoecology 13:129–134CrossRefGoogle Scholar
  28. Kikuta N, Tsuji K (1999) Queen and worker policing in the monogynous and monandrous ant, Diacamma sp. Behav Ecol Sociobiol 46:180–189CrossRefGoogle Scholar
  29. Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557–560PubMedCrossRefGoogle Scholar
  30. Lorenzi MC, Filippone F (2000) Opportunistic discrimination of alien eggs by social wasps (Polistes biglumis, Hymenoptera Vespidae): a defense against social parasitism? Behav Ecol Sociobiol 48:402–406CrossRefGoogle Scholar
  31. Martin SJ, Jones GR, Châline N, Middleton H, Ratnieks FLW (2002) Reassessing the role of the honeybee (Apis mellifera) Dufour’s gland in egg marking. Naturwissenschaften 89:528–532PubMedCrossRefGoogle Scholar
  32. Martin SJ, Châline N, Oldroyd BP, Jones GR, Ratnieks FLW (2004) Egg marking pheromones of anarchistic worker honeybees (Apis mellifera). Behav Ecol 15:839–844CrossRefGoogle Scholar
  33. Montague CE, Oldroyd BP (1998) The evolution of worker sterility in honey bees: an investigation into a behavioral mutant causing a failure of worker policing. Evolution 52:1408–1415CrossRefGoogle Scholar
  34. Nanork P, Paar J, Chapman NC, Wongsiri S, Oldroyd BP (2005) Asian honey bees parasitize the future dead. Nature 437:829PubMedCrossRefGoogle Scholar
  35. Nanork P, Wongsiri S, Oldroyd BP (2006) The reproductive dilemmas of queenless red dwarf honey bee (Apis florea) workers. Behav Ecol Sociobiol 61:91–97CrossRefGoogle Scholar
  36. Nanork P, Chapman NC, Wongsiri S, Lim JA, Gloag R, Oldroyd BP (2007) Social parasitism by workers in queenless and queenright Apis cerana colonies. Mol Ecol 16:1107–1114PubMedCrossRefGoogle Scholar
  37. Oldroyd BP, Ratnieks FLW (2000) Anarchistic honey bee workers evade worker policing by laying eggs that have low removal rates. Behav Ecol Sociobiol 47:268–273CrossRefGoogle Scholar
  38. Oldroyd BP, Wongsiri S (2006) Asian honey bees. Biology, conservation and human interactions. Harvard University Press, Cambridge, MAGoogle Scholar
  39. Oldroyd BP, Smolenski AJ, Cornuet J-M, Crozier RH (1994) Anarchy in the beehive. Nature 371:749CrossRefGoogle Scholar
  40. Oldroyd BP, Smolenski AJ, Cornuet J-M, Wongsiri S, Estoup A, Rinderer TE, Crozier RH (1996) Levels of polyandry and intracolonial genetic relationships in Apis dorsata (Hymenoptera: Apidae). Ann Entomol Soc Am 89:276–283Google Scholar
  41. Oldroyd BP, Halling LA, Good G, Wattanachaiyingchareon W, Barron AB, Nanork P, Wongsiri S, Ratnieks FLW (2001) Worker policing and worker reproduction in Apis cerana. Behav Ecol Sociobiol 50:371–377CrossRefGoogle Scholar
  42. Oldroyd BP, Ratnieks FLW, Wossler TC (2002) Egg marking pheromones in honey bees Apis mellifera. Behav Ecol Sociobiol 51:590–591CrossRefGoogle Scholar
  43. Raffiudin R, Crozier RH (2006) Phylogenetic analysis of honey bee behavioral evolution. Mol Phylogenet Evol (in press). DOI  10.1016/j.ympev.2006.10.103
  44. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236CrossRefGoogle Scholar
  45. Ratnieks FLW (1995) Evidence for queen-produced egg-marking pheromone and its use in worker policing in the honey bee. J Apic Res 34:31–37Google Scholar
  46. Ratnieks FLW, Visscher PK (1989) Worker policing in honeybees. Nature 342:796–797CrossRefGoogle Scholar
  47. Ratnieks FLW, Wenseleers T (2005) Policing insect societies. Science 307:54–56PubMedCrossRefGoogle Scholar
  48. Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608PubMedCrossRefGoogle Scholar
  49. Sole CL, Kryger P, Hefetz A, Katzav-Gozansky T, Crewe RM (2002) Mimicry of queen Dufour’s gland secretions by workers of Apis mellifera scutellata and A. m. capensis. Naturwissenschaften 89:561–564PubMedGoogle Scholar
  50. Taber S (1961) Forceps designed for transferring honey bee eggs. J Econ Entomol 54:247–250Google Scholar
  51. Wattanachaiyingcharoen W, Oldroyd BP, Good G, Halling LA, Ratnieks FLW, Wongsiri S (2001) Lack of worker reproduction in Apis dorsata. Insectes Soc 49:80–85CrossRefGoogle Scholar
  52. Wenseleers T, Hart AG, Ratnieks FLW (2004a) When resistance is useless: Policing and the evolution of reproductive acquiescence in insect societies. Am Nat 164:E154–E167CrossRefGoogle Scholar
  53. Wenseleers T, Helanterä H, Hart A, Ratnieks FLW (2004b) Worker reproduction and policing in insect societies: an ESS analysis. J Evol Biol 17:1035–1047PubMedCrossRefGoogle Scholar
  54. Wenseleers T, Ratnieks FLW (2006a) Comparative analysis of worker reproduction and policing in Eusocial Hymenoptera supports policing theory. Am Nat 168:E163–E179PubMedCrossRefGoogle Scholar
  55. Wenseleers T, Ratnieks FLW (2006b) Enfrced altruism in insect societies. Nature 444:50PubMedCrossRefGoogle Scholar
  56. Wenseleers T, Badcock NS, Erven K, Tofilski A, Nascimento FS, Hart AG, Burke TA, Archer ME, Ratnieks FLW (2005) A test of worker policing theory in an advanced eusocial wasp, Vespula rufa. Evolution 59:1306–1314PubMedGoogle Scholar
  57. Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge, MAGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Piyamas Nanork
    • 1
  • Siriwat Wongsiri
    • 2
  • Benjamin P. Oldroyd
    • 3
  1. 1.Department of BiologyMahasarakham UniversityMahasarakhamThailand
  2. 2.Faculty of TechnologyMahasarakham UniversityMahasarakhamThailand
  3. 3.Behaviour and Genetics of Social Insects Laboratory, School of Biological SciencesUniversity of SydneySydneyAustralia

Personalised recommendations