Behavioral Ecology and Sociobiology

, Volume 55, Issue 6, pp 513–523 | Cite as

Levels of selection in a social insect: a review of conflict and cooperation during honey bee (Apis mellifera) queen replacement

  • David R. TarpyEmail author
  • David C. Gilley
  • Thomas D. Seeley


The extended phenotype of a social insect colony enables selection to act at both the individual level (within-colony selection) and the colony level (between-colony selection). Whether a particular trait persists over time depends on the relative within- and between-colony selection pressures. Queen replacement in honey bee colonies exemplifies how selection may act at these different levels in opposing directions. Normally, a honey bee colony has only one queen, but a colony rears many new queens during the process of colony reproduction. The replacement of the mother queen has two distinct phases: queen rearing, where many queens develop and emerge from their cells, and queen elimination, where most queens die in a series of fatal duels. Which queens are reared to adulthood and which queens ultimately survive the elimination process depends on the strength and direction of selection at both the individual and colony levels. If within-colony selection is predominant, then conflict is expected to occur among nestmates over which queens are produced. If between-colony selection is predominant, then cooperation is expected among nestmates. We review the current evidence for conflict and cooperation during queen replacement in honey bees during both the queen rearing and queen elimination phases. In particular, we examine whether workers of different subfamilies exhibit conflict by acting nepotistically toward queens before and after they have emerged from their cells, and whether workers exhibit cooperation by collectively producing queens of high reproductive quality. We conclude that although workers may weakly compete through nepotism during queen rearing, workers largely cooperate to raise queens of similar reproductive potential so that any queen is suitable to inherit the nest. Thus it appears that potential conflict over queen replacement in honey bees has not translated into actual conflict, suggesting that between-colony selection predominates during these important events in a colony’s life cycle.


Polygyny Nepotism Colony reproduction Reproductive conflict Levels of selection 



We thank H.K. Reeve for his input and support in this project, as well as S.S. Schneider for providing unpublished results and suggestions for the manuscript. We also thank A. Cockburn for his comments on the manuscript. Funding was provided to D.R.T. by USDA grant 35302-09905 and NSF grant IBN-973-4181, to D.C.G. by NSF grant 0104929, and to T.D.S. by USDA Hatch grant NYC-191407.


  1. Allen MD (1956) The behavior of honeybees preparing to swarm. Anim Behav 4:14–22Google Scholar
  2. Arnqvist G, Wooster D (1995) Meta-analysis: synthesizing research findings in ecology and evolution. Trends Ecol Evol 10:236–240CrossRefGoogle Scholar
  3. Avetisyan GA (1961) The relation between interior and exterior characteristics of the queen and fertility and productivity of the bee colony. In: XVIII International Beekeeping Congress, Madrid, Spain, pp 44–53Google Scholar
  4. Balas MT, Adams ES (1996) The dissolution of cooperative groups: mechanisms of queen mortality in incipient fire ant colonies. Behav Ecol Sociobiol 38:391–399CrossRefGoogle Scholar
  5. Bernasconi G, Keller L (1996) Reproductive conflicts in cooperative associations of fire ant queens (Solenopsis invicta). Proc R Soc Lond B 263:509–513Google Scholar
  6. Bernasconi G, Krieger MJB, Keller L (1997) Unequal partitioning of reproduction and investment between cooperating queens in the fire ant, Solenopsis invicta, as revealed by microsatellites. Proc R Soc Lond B 264:1331–1336CrossRefGoogle Scholar
  7. Bernasconi G, Ratnieks FLW, Rand E (2000) Effect of “spraying” by fighting honey bee queens (Apis mellifera L.) on the temporal structure of fights. Insectes Soc 47:21–26CrossRefGoogle Scholar
  8. Boch R (1979) Queen substance pheromone produced by immature queen honeybees. J Apic Res 18:12–15Google Scholar
  9. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton, N.J.Google Scholar
  10. Breed MD (1998) Recognition pheromones of the honey bee. Bioscience 48:463–470Google Scholar
  11. Breed MD, Velthuis HHW, Robinson GE (1984) Do worker honey bees discriminate among unrelated and related larval phenotypes? Ann Entomol Soc Am 77:737–739Google Scholar
  12. Breed MD, Welch CK, Cruz R (1994) Kin discrimination within honey bee (Apis mellifera) colonies: an analysis of the evidence. Behav Process 33:25–40CrossRefGoogle Scholar
  13. Carlin NF, Reeve HK, Cover SP (1993) Kin discrimination and division of labour among matrilines in the polygynous carpenter ant, Camponotus planatus. In: Keller L (ed) Queen number and sociality in insects. Oxford University Press, Oxford, pp 362–401Google Scholar
  14. Châline N, Arnold G, Papin C, Ratnieks FLW (2003) Patriline differences in emergency queens rearing in the honey bee, Apis mellifera. Insectes Soc 50:234–236CrossRefGoogle Scholar
  15. Clarke RJ (1989) Queen physiological quality. A discussion paper for New Zealand queen producers. Sunflora Apiaries, Blenheim, New Zealand, pp 1–9Google Scholar
  16. Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, OxfordGoogle Scholar
  17. Darwin C (1859) On the origin of species. Murray, LondonGoogle Scholar
  18. Dawkins R (1982) The extended phenotype. Freeman, OxfordGoogle Scholar
  19. Dawkins R (1989) The selfish gene, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  20. DeGrandi-Hoffman G, Watkins JC, Collins AM, Loper GM, Martin JH, Arias MC, Sheppard WS (1998) Queen developmental time as a factor in the Africanization of European honey bee (Hymenoptera: Apidae) populations. Ann Entomol Soc Am 91:52–58Google Scholar
  21. Eckert JE (1934) Studies in the number of ovarioles in queen honeybees in relation to body size. J Econ Entomol 27:629–635Google Scholar
  22. Estoup A, Solignac M, Cornuet J (1994) Precise assessment of the number of patrilines and of genetic relatedness in honeybee colonies. Proc R Soc Lond B 258:1–7Google Scholar
  23. Fell RD, Morse RA (1984) Emergency queen cell production in the honey bee colony. Insectes Soc 31:221–237Google Scholar
  24. Fletcher DJC (1978) Vibration of queen cells by worker honeybees and its relation to the issue of swarms with virgin queens. J Apic Res 17:14–26Google Scholar
  25. Fletcher DJC, Ross KG (1985) Regulation of reproduction in eusocial Hymenoptera. Annu Rev Entomol 30:319–343CrossRefGoogle Scholar
  26. Frank P, Solignac M, Vautrin D, Cornuet J-M, Koeniger G, Koeniger N (2002) Sperm competition and last-male precedence in the honeybee. Anim Behav 64:503–509CrossRefGoogle Scholar
  27. Futuyma DJ (1998) Evolutionary biology. Sinauer, Sunderland, Mass.Google Scholar
  28. Gary NE, Morse RA (1962) The events following queen cell construction in honeybee colonies. J Apic Res 1:3–5Google Scholar
  29. Gilley DC (2001) The behavior of honey bees (Apis mellifera ligustica) during queen duels. Ethology 107:601–622CrossRefGoogle Scholar
  30. Gilley DC (2003) Absence of nepotism in the aggressive interactions between workers and dueling queen honey bees. Proc R Soc Lond B. 270:2045–2049Google Scholar
  31. Gilley DC, Tarpy DR, Land BB (2003) The effect of queen quality on the interactions of workers and dueling queen honey bees (Apis mellifera L.). Behav Ecol Sociobiol 55:190–196Google Scholar
  32. Griffin AS, West SA (2002) Kin selection: fact and fiction. Trends Ecol Evol 17:15–21CrossRefGoogle Scholar
  33. Grooters HJ (1987) Influences of queen piping and worker behaviour on the timing of emergence of honey bee queens. Insectes Soc 34:181–193Google Scholar
  34. Hamilton WD (1964) The genetical evolution of social behaviour. I and II. J Theoret Biol 7:1–52Google Scholar
  35. Hannonen M, Sundström L (2003) Worker nepotism among polygynous ants. Nature 421:910–910CrossRefPubMedGoogle Scholar
  36. Hatch S, Tarpy DR, Fletcher DJC (1999) Worker regulation of emergency queen rearing in honey bee colonies and the resultant variation in queen quality. Insectes Soc 46:372–377CrossRefGoogle Scholar
  37. Heinze J (1993) Queen–queen interactions in polygynous ants. In: Keller L (ed) Queen number and sociality in insects. Oxford University Press, New York, pp 334–361Google Scholar
  38. Herbert EW Jr (1992) Honey bee nutrition. In: The hive and the honey bee. Dadant, Hamilton, Ill., pp 197–233Google Scholar
  39. Huber F (1926) New observations on bees, vol 1. Translated from the French by C.P. Dadant. American Bee Journal, Hamilton IL [First published in 1792]Google Scholar
  40. Keller L (1999) Levels of selection in evolution. Princeton University Press, Princeton, N.J.Google Scholar
  41. Keller L, Reeve HK (1999) Dynamics of conflicts in insect societies. In: Keller L (ed) Levels of selection in evolution. Princeton University Press, Princeton, N.J., pp 153–175Google Scholar
  42. Kirchner WH (1993) Vibrational signals in the tremble dance of the honeybee, Apis mellifera. Behav Ecol Sociobiol 33:169–172Google Scholar
  43. Laidlaw HH Jr, Page RE Jr (1997) Queen rearing and bee breeding. Wicwas, Cheshire, Conn.Google Scholar
  44. Makarov YI (1969) Biologically and economically useful characters of far eastern bees and their selection. PhD thesis, Timiryazev Academy of Agriculture, MoscowGoogle Scholar
  45. Melathopoulos AP, Winston ML, Pettis JS, Pankiw T (1996) Effect of queen mandibular pheromone on initiation and maintenance of queen cells in the honey bee (Apis mellifera L.). Can Entomol 128:263–272Google Scholar
  46. Michener C, D, (1974) The social behavior of the bees. Harvard University Press, Cambridge, Mass.Google Scholar
  47. Mohammedi A, Le Conte Y (2000) Do environmental conditions exert an effect on nest-mate recognition in queen rearing honey bees? Insectes Soc 47:307–312Google Scholar
  48. Moritz RFA (1985) The effects of multiple mating on the worker-queen conflict in Apis mellifera. Behav Ecol Sociobiol 16:1986Google Scholar
  49. Noonan KC (1986) Recognition of queen larvae by worker honey bees (Apis mellifera). Ethology 73:295–306Google Scholar
  50. Oldroyd BP, Clifton MJ, Parker K, Wongsiri S, Rinderer TE, Crozier RH (1998) Evolution of mating behavior in the genus Apis and an estimate of mating frequency in Apis cerana (Hymenoptera: Apidae). Ann Entomol Soc Am 91:700–709Google Scholar
  51. Oldroyd BP, Rinderer TE, Buco SM (1990) Nepotism in the honey bee. Nature 346:707–708CrossRefGoogle Scholar
  52. Osborne KE, Oldroyd BP (1999) Possible causes of reproductive dominance during emergency queen rearing by honeybees. Anim Behav 58:267–272CrossRefPubMedGoogle Scholar
  53. Page RE Jr, Erickson EH (1984) Selective queen rearing by worker honeybees: kin or nestmate recognition. Ann Entomol Soc Am 77:578–580Google Scholar
  54. Page RE Jr, Erickson EH Jr (1986a) Kin recognition during emergency queen rearing by worker honey bees (Hymenoptera: Apidae). Ann Entomol Soc Am 79:460–467Google Scholar
  55. Page RE Jr, Erickson EH (1986b) Kin recognition of virgin queen acceptance by worker honey bees (Apis mellifera L.). Anim Behav 34:1061–1069Google Scholar
  56. Page RE Jr, Peng CYS (2001) Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp Gerontol 36:695–711PubMedGoogle Scholar
  57. Page RE Jr, Blum MS, Fales HM (1988) o-Aminoacetophenone, a pheromone that repels honeybees (Apis mellifera L.). Experientia 44:270–271PubMedGoogle Scholar
  58. Page RE Jr, Robinson GE, Fondrk MK (1989) Genetic specialists, kin recognition and nepotism in honeybee colonies. Nature 339:576–579CrossRefGoogle Scholar
  59. Pankiw T (1997) Queen rearing by high and low queen mandibular pheromone responding worker honey bees (Apis mellifera L.). Can Entomol 129:679–690Google Scholar
  60. Post DC, Page RE Jr, Erickson EH (1987) Honeybee (Apis mellifera L.) queen feces: source of a pheromone that repels worker bees. J Chem Ecol 13:583–591Google Scholar
  61. Queller DC, Strassmann JE (2002) The many selves of social insects. Science 296:311–313CrossRefPubMedGoogle Scholar
  62. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial hymenoptera. Am Nat 132:217–236CrossRefGoogle Scholar
  63. Ratnieks FLW (1989) Conflict and cooperation in insect societies. PhD thesis, Cornell University, Ithaca, N.Y.Google Scholar
  64. 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
  65. Robinson GE, Page RE, Jr., Arensen N (1994) Genotypic differences in brood rearing in honey bee colonies: context-specific? Behav Ecol Sociobiol 34:125–137CrossRefGoogle Scholar
  66. Schmickl T, Crailsheim K (2002) How honeybees (Apis mellifera L.) change their broodcare behaviour in response to non-foraging conditions and poor pollen conditions. Behav Ecol Sociobiol 51:415–425CrossRefGoogle Scholar
  67. Schneider SS, DeGrandi-Hoffman G (2002) The influence of worker behavior and paternity on the development and emergence of honey bee queens. Insectes Soc 49:306–314Google Scholar
  68. Schneider SS, DeGrandi-Hoffman G (2003) The influence of paternity on virgin queen success in hybrid colonies of European and African honeybees. Anim Behav 65:883–892CrossRefGoogle Scholar
  69. Schneider SS, Painter Kurt S, Degrandi-Hoffman G (2001) The role of the vibration signal during queen competition in colonies of the honeybee, Apis mellifera. Anim Behav 61:1173–1180CrossRefGoogle Scholar
  70. Sundström L, Boomsma JJ (2001) Conflicts and alliances in insect families. Heredity 86:515–521CrossRefPubMedGoogle Scholar
  71. Tarpy DR, Fletcher DJC (1998) Effects of relatedness on queen competition within honey bee colonies. Anim Behav 55:537–543CrossRefPubMedGoogle Scholar
  72. Tarpy DR, Fletcher DJC (2003) ‘Spraying’ behavior during queen competition in honey bees. J Insect Behav 16:425–437CrossRefGoogle Scholar
  73. Tarpy DR, Nielsen DI (2002) Sampling error, effective paternity, and estimating the genetic structure of honey bee colonies (Hymenoptera:Apidae). Ann Entomol Soc Am 95:513–528Google Scholar
  74. Tarpy DR, Hatch S, Fletcher DJC (2000) The influence of queen age and quality during queen replacement in honeybee colonies. Anim Behav 59:97–101CrossRefPubMedGoogle Scholar
  75. Tilley CA, Oldroyd BP (1997) Unequal subfamily proportions among honey bee queen and worker brood. Anim Behav 54:1483–1490CrossRefPubMedGoogle Scholar
  76. Visscher PK (1986) Kinship discrimination in queen rearing by honey bees (Apis mellifera). Behav Ecol Sociobiol 18:453–460Google Scholar
  77. Visscher PK (1993) A theoretical analysis of individual interests and intracolony conflict during swarming of honey bee colonies. J Theor Biol 165:191–212CrossRefGoogle Scholar
  78. Visscher PK (1998) Colony integration and reproductive conflict in honey bees. Apidologie 29:23–45Google Scholar
  79. Wilson DS (1997) Multilevel selection theory comes of age—introduction. Am Nat 150:S1–S4CrossRefGoogle Scholar
  80. Wilson EO (1971) The insect societies. Harvard University Press, Cambridge, Mass.Google Scholar
  81. Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge, Mass.Google Scholar
  82. Winston ML, Taylor OR (1980) Factors preceding queen rearing in the Africanized honeybee (Apis melifera) in South America. Insectes Soc 27:289–304Google Scholar
  83. Woyciechowski M (1990) Do honey bee, Apis mellifera L., workers favour sibling eggs and larvae in queen rearing? Anim Behav 39:1220–1222Google Scholar
  84. Woyciechowski M, Lomnicki A (1987) Multiple mating of queens and the sterility of workers among eusocial Hymenoptera. J Theor Biol 128:317–328Google Scholar
  85. Woyke J (1971) Correlations between the age at which honeybee brood was grafted, characteristics of the resultant queens, and results of insemination. J Apic Res 10:45–55Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • David R. Tarpy
    • 1
    Email author
  • David C. Gilley
    • 2
  • Thomas D. Seeley
    • 3
  1. 1.Department of EntomologyNorth Carolina State UniversityRaleighUSA
  2. 2.Carl Hayden Bee Research CenterTucsonUSA
  3. 3.Department of Neurobiology and BehaviorCornell UniversityIthacaUSA

Personalised recommendations