Behavioral Ecology and Sociobiology

, Volume 58, Issue 1, pp 80–86 | Cite as

Queen and worker policing in the tree wasp Dolichovespula sylvestris

Original Article

Abstract

Insect societies are sometimes exploited by workers who reproduce selfishly rather than help to rear the queen’s offspring. This causes a conflict-of-interest with the mother queen and, frequently, with the non-reproductive workers as well. One mechanism that can reduce conflict is policing, whereby either the queen or other workers aggress egg-laying workers or destroy worker-laid eggs. Here we present the first direct observations of queen and worker policing in natural, unmanipulated colonies of a social insect, the tree wasp Dolichovespula sylvestris. Worker reproduction was common, with workers producing 50% of all male eggs. However, most worker-laid eggs, 91%, were policed within 1 day, whereas most queen-laid eggs, 96%, remained unharmed. The workers were responsible for 51% of all policing events and the queen for 49%. The workers and mother queen also commonly aggressed ovipositing workers, and successfully prevented them from depositing eggs in 14% and 6% of all attempted ovipositions. Hence, both queen policing and worker policing occur and policing acts via two distinct mechanisms: selective destruction of worker-laid eggs and aggression of ovipositing workers. At a general level, our study shows that both centralized and decentralized control can act together to suppress conflict within social groups.

Keywords

Social policing Reproductive conflict Social insects Vespinae Dolichovespula sylvestris 

References

  1. Archer ME (2002) A numerical account of the development of colonies of the social wasp, Dolichovespula sylvestris (Scopoli) (Hym., Vespinae), in England and overseas. Entomol Mon Mag 138:209–224Google Scholar
  2. 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
  3. Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Q Rev Biol 63:291–311CrossRefGoogle Scholar
  4. Bourke AFG (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257CrossRefGoogle Scholar
  5. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton, N.J.Google Scholar
  6. Bourke AFG, Ratnieks FLW (1999) Kin conflict over caste determination in social Hymenoptera. Behav Ecol Sociobiol 46:287–297CrossRefGoogle Scholar
  7. Clutton-Brock TH, Parker GA (1995) Punishment in animal societies. Nature 373:209–216CrossRefPubMedGoogle Scholar
  8. Cnaani J, Schmid-Hempel R, Schmidt JO (2002) Colony development, larval development and worker reproduction in Bombus impatiens Cresson. Insectes Soc 49:164–170CrossRefGoogle Scholar
  9. Cole BJ (1984) Colony efficiency and the reproductivity effect in Leptothorax allardycei (Mann). Insectes Soc 31:403–407Google Scholar
  10. Cole BJ (1986) The social behavior of Leptothorax allardycei (Hymenoptera, formicidae): time budgets and the evolution of worker reproduction. Behav Ecol Sociobiol 18:165–173CrossRefGoogle Scholar
  11. Crozier RH, Pamilo P (1996) Evolution of social insect colonies. Sex allocation and kin selection. Oxford University Press, OxfordGoogle Scholar
  12. D’Ettorre P, Heinze J, Ratnieks FLW (2004) Worker policing by egg-eating in the ponerine ant Pachycondyla inversa. Proc R Soc Lond Ser B Biol Sci 271:1427–1434CrossRefGoogle Scholar
  13. Edwards R (1980) Social wasps: their biology and control. Rentokil, East GrinsteadGoogle Scholar
  14. Fletcher DJC, Ross KG (1985) Regulation of reproduction in eusocial Hymenoptera. Annu Rev Entomol 30:319–343CrossRefGoogle Scholar
  15. Foster KR, Ratnieks FLW (2000) Facultative worker policing in a wasp. Nature 407:692–693CrossRefGoogle Scholar
  16. Foster KR, Ratnieks FLW (2001a) Convergent evolution of worker policing by egg eating in the honeybee and common wasp. Proc R Soc Lond Ser B Biol Sci 268:169–174Google Scholar
  17. Foster KR, Ratnieks FLW (2001b) The effect of sex-allocation biasing on the evolution of worker policing in hymenopteran societies. Am Nat 158:615–623CrossRefGoogle Scholar
  18. Foster KR, Ratnieks FLW (2001c) Paternity, reproduction and conflict in vespine wasps: a model system for testing kin selection predictions. Behav Ecol Sociobiol 50:1–8CrossRefGoogle Scholar
  19. Foster KR, Ratnieks FLW, Gyllenstrand N, Thoren PA (2001) Colony kin structure and male production in Dolichovespula wasps. Mol Ecol 10:1003–1010CrossRefGoogle Scholar
  20. Foster KR, Gulliver J, Ratnieks FLW (2002) Worker policing in the European hornet Vespa crabro. Insectes Soc 49:41–44CrossRefGoogle Scholar
  21. Free JB, Weinberg I, Whiten A (1969) The egg-eating behaviour of Bombus lapidarius L. Behaviour 35:313–317Google Scholar
  22. Gobin B, Billen J, Peeters C (1999) Policing behaviour towards virgin egg layers in a polygynous ponerine ant. Anim Behav 58:1117–1122PubMedGoogle Scholar
  23. Greene A (1979) Behavioural characters as indicators of yellowjacket phylogeny (Hymenoptera: Vespidae). Ann Entomol Soc Am 72:614–619Google Scholar
  24. 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
  25. Hammond RL, Keller L (2004) Conflict over male parentage in social insects. PLoS Biol 2:1–11CrossRefGoogle Scholar
  26. Hardin G (1968) The tragedy of the commons. Science 162:1243–1244Google Scholar
  27. Hartmann A, Heinze J (2003) Lay eggs, live longer: division of labor and life span in a clonal ant species. Evolution 57:2424–2429Google Scholar
  28. Hillesheim E, Koeniger N, Moritz RFA (1989) Colony performance in honeybees (Apis mellifera capensis Esch) depends on the proportion of subordinate and dominant workers. Behav Ecol Sociobiol 24:291–296CrossRefGoogle Scholar
  29. Hofer H (1998) The Hutterites: lives and images of a communal people. Hofer, Saskatoon, SK, CanadaGoogle Scholar
  30. Kikuta N, Tsuji K (1999) Queen and worker policing in the monogynous and monandrous ant, Diacamma sp. Behav Ecol Sociobiol 46:180–189CrossRefGoogle Scholar
  31. Landolt PJ, Akre RD, Greene A (1977) Effects of colony division on Vespula atropilosa (Sladen) (Hymenoptera: Vespidae). J Kansas Entomol Soc 50:135–147Google Scholar
  32. Lee ET, Wang JW (2003) Statistical methods for survival data analysis, 3rd edn. Wiley, New YorkGoogle Scholar
  33. Martin SJ, Beekman M, Wossler TC, Ratnieks FLW (2002) Parasitic Cape honeybee workers, Apis mellifera capensis, evade policing. Nature 415:163–165PubMedGoogle Scholar
  34. Michener CD, Brothers DJ (1974) Were workers of eusocial Hymenoptera initially altruistic or oppressed? Proc Natl Acad Sci USA 71:671–674Google Scholar
  35. Mock DW, Parker G (1998) The evolution of sibling rivalry. Oxford University Press, OxfordGoogle Scholar
  36. Monnin T, Peeters C (1997) Cannibalism of subordinates’ eggs in the monogynous queenless ant Dinoponera quadriceps. Naturwissenschaften 84:499–502CrossRefGoogle Scholar
  37. Moritz RFA, Hillesheim E (1985) Inheritance of dominance in honeybees (Apis mellifera capensis Esch). Behav Ecol Sociobiol 17:87–89CrossRefGoogle Scholar
  38. Nakata K, Tsuji K (1996) The effect of colony size on conflict over male-production between gamergate and dominant workers in the ponerine ant Diacamma sp. Ethol Ecol Evol 8:147–156Google Scholar
  39. Pomeroy N (1979) Brood bionomics of Bombus ruderatus in New Zealand (Hymenoptera: Apidae). Can Entomol 111:865–874Google Scholar
  40. Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165–175Google Scholar
  41. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236CrossRefGoogle Scholar
  42. Ratnieks FLW (1993) Egg-laying, egg-removal, and ovary development by workers in queenright honey-bee colonies. Behav Ecol Sociobiol 32:191–198CrossRefGoogle Scholar
  43. Ratnieks FLW (1995) Evidence for a queen-produced egg-marking pheromone and its use in worker policing in the honey-bee. J Apic Res 34:31–37Google Scholar
  44. Ratnieks FLW (2000) Worker policing in the honey bee: basic facts and ideas. Insect Social Life 3:3–10Google Scholar
  45. Ratnieks FLW, Reeve HK (1992) Conflict in single-queen hymenopteran societies—the structure of conflict and processes that reduce conflict in advanced eusocial species. J Theor Biol 158:33–65Google Scholar
  46. Ratnieks FLW, Visscher PK (1989) Worker policing in the honeybee. Nature 342:796–797CrossRefGoogle Scholar
  47. Ratnieks FLW, Wenseleers T (2005) Policing insect societies. Science 307: 54–56CrossRefGoogle Scholar
  48. Ross KG (1985) Aspects of worker reproduction in 4 social wasp species (Insecta, Hymenoptera, Vespidae). J Zool 205:411–424Google Scholar
  49. Saigo T, Tsuchida K (2004) Queen and worker policing in monogynous and monandrous colonies of a primitively eusocial wasp. Proc R Soc Lond Ser B Biol Sci [Suppl] 271:S509–S512Google Scholar
  50. Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences, 2nd edn. McGraw-Hill, New YorkGoogle Scholar
  51. Spradbery JP (1991) Evolution of queen number and queen control. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Comstock, Pa., pp 336–388Google Scholar
  52. Starr CK (1984) Sperm competition, kinship, and sociality: a review of modern theory. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, Orlando, pp 427–464Google Scholar
  53. Statsoft I (1995) STATISTICA for Windows (computer program manual). StatSoft, 2300 East 14th Street, Tulsa, Okla., http://www.statsoft.com
  54. Tóth E, Queller DC, Dollin A, Strassmann JE (2004) Conflict over male parentage in stingless bees. Insectes Soc 51:1–11CrossRefGoogle Scholar
  55. Tóth E, Strassmann JE, Nogueira-Neto P, Imperatriz-Fonseca VL, Queller DC (2002) Male production in stingless bees: variable outcomes of queen–worker conflict. Mol Ecol 11:2661–2667CrossRefGoogle Scholar
  56. Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249–263PubMedGoogle Scholar
  57. Visscher PK (1996) Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing. Behav Ecol Sociobiol 39:237–244CrossRefGoogle Scholar
  58. Wenseleers T, Ratnieks FLW (2004) Tragedy of the commons in Melipona bees. Proc R Soc Lond Ser B Biol Sci [Suppl] 271:S310-S312Google Scholar
  59. Wenseleers T, Ratnieks FLW, Billen J (2003) Caste fate conflict in swarm-founding social Hymenoptera: an inclusive fitness analysis. J Evol Biol 16:647–658CrossRefGoogle Scholar
  60. 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
  61. Wenseleers T, Hart AG, Ratnieks FLW, Quezada-Euan JJG (2004b) Queen execution and caste conflict in the stingless bee Melipona beecheii. Ethology 110:725–736CrossRefGoogle Scholar
  62. Wenseleers T, Helanterä H, Hart AG, Ratnieks FLW (2004c) Worker reproduction and policing in insect societies. An ESS analysis. J Evol Biol 17:1035–1047CrossRefPubMedGoogle Scholar
  63. Wilson EO (1971) The insect societies. Harvard University Press, Cambridge, Mass.Google Scholar
  64. Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge, Mass.Google Scholar
  65. Woyciechowski M, Lomnicki A (1987) Multiple mating of queens and the sterillity of workers among eusocial Hymenoptera. J Theor Biol 128:317–327Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • T. Wenseleers
    • 1
    • 2
  • A. Tofilski
    • 3
  • F. L. W. Ratnieks
    • 2
    • 3
  1. 1.Laboratory of Entomology, Zoological InstituteUniversity of LeuvenLeuvenBelgium
  2. 2.Wissenschaftskolleg zu Berlin (Institute for Advanced Study) BerlinBerlinGermany
  3. 3.Laboratory of Apiculture and Social Insects, Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK

Personalised recommendations