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

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Abstract

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.

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References

  • Allen MD (1956) The behavior of honeybees preparing to swarm. Anim Behav 4:14–22

    Google Scholar 

  • Arnqvist G, Wooster D (1995) Meta-analysis: synthesizing research findings in ecology and evolution. Trends Ecol Evol 10:236–240

    Article  Google Scholar 

  • 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 44–53

  • Balas MT, Adams ES (1996) The dissolution of cooperative groups: mechanisms of queen mortality in incipient fire ant colonies. Behav Ecol Sociobiol 38:391–399

    Article  Google Scholar 

  • Bernasconi G, Keller L (1996) Reproductive conflicts in cooperative associations of fire ant queens (Solenopsis invicta). Proc R Soc Lond B 263:509–513

    Google Scholar 

  • 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 264:1331–1336

    Article  Google Scholar 

  • 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 47:21–26

    Article  Google Scholar 

  • Boch R (1979) Queen substance pheromone produced by immature queen honeybees. J Apic Res 18:12–15

    CAS  Google Scholar 

  • Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton, N.J.

  • Breed MD (1998) Recognition pheromones of the honey bee. Bioscience 48:463–470

    Google Scholar 

  • Breed MD, Velthuis HHW, Robinson GE (1984) Do worker honey bees discriminate among unrelated and related larval phenotypes? Ann Entomol Soc Am 77:737–739

    Google Scholar 

  • Breed MD, Welch CK, Cruz R (1994) Kin discrimination within honey bee (Apis mellifera) colonies: an analysis of the evidence. Behav Process 33:25–40

    Article  Google Scholar 

  • 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 362–401

  • Châline N, Arnold G, Papin C, Ratnieks FLW (2003) Patriline differences in emergency queens rearing in the honey bee, Apis mellifera. Insectes Soc 50:234–236

    Article  Google Scholar 

  • Clarke RJ (1989) Queen physiological quality. A discussion paper for New Zealand queen producers. Sunflora Apiaries, Blenheim, New Zealand, pp 1–9

  • Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, Oxford

    Google Scholar 

  • Darwin C (1859) On the origin of species. Murray, London

  • Dawkins R (1982) The extended phenotype. Freeman, Oxford

  • Dawkins R (1989) The selfish gene, 2nd edn. Oxford University Press, Oxford

  • 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 91:52–58

    Google Scholar 

  • Eckert JE (1934) Studies in the number of ovarioles in queen honeybees in relation to body size. J Econ Entomol 27:629–635

    Google Scholar 

  • 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 258:1–7

    CAS  Google Scholar 

  • Fell RD, Morse RA (1984) Emergency queen cell production in the honey bee colony. Insectes Soc 31:221–237

    Google Scholar 

  • Fletcher DJC (1978) Vibration of queen cells by worker honeybees and its relation to the issue of swarms with virgin queens. J Apic Res 17:14–26

    Google Scholar 

  • Fletcher DJC, Ross KG (1985) Regulation of reproduction in eusocial Hymenoptera. Annu Rev Entomol 30:319–343

    Article  Google Scholar 

  • 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 64:503–509

    Article  Google Scholar 

  • Futuyma DJ (1998) Evolutionary biology. Sinauer, Sunderland, Mass.

  • Gary NE, Morse RA (1962) The events following queen cell construction in honeybee colonies. J Apic Res 1:3–5

    Google Scholar 

  • Gilley DC (2001) The behavior of honey bees (Apis mellifera ligustica) during queen duels. Ethology 107:601–622

    Article  Google Scholar 

  • Gilley DC (2003) Absence of nepotism in the aggressive interactions between workers and dueling queen honey bees. Proc R Soc Lond B. 270:2045–2049

    Google Scholar 

  • 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 55:190–196

    Google Scholar 

  • Griffin AS, West SA (2002) Kin selection: fact and fiction. Trends Ecol Evol 17:15–21

    Article  Google Scholar 

  • Grooters HJ (1987) Influences of queen piping and worker behaviour on the timing of emergence of honey bee queens. Insectes Soc 34:181–193

    Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. I and II. J Theoret Biol 7:1–52

    CAS  Google Scholar 

  • Hannonen M, Sundström L (2003) Worker nepotism among polygynous ants. Nature 421:910–910

    Article  CAS  PubMed  Google Scholar 

  • 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 46:372–377

    Article  Google Scholar 

  • 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 334–361

  • Herbert EW Jr (1992) Honey bee nutrition. In: The hive and the honey bee. Dadant, Hamilton, Ill., pp 197–233

  • 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]

  • Keller L (1999) Levels of selection in evolution. Princeton University Press, Princeton, N.J.

  • 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 153–175

  • Kirchner WH (1993) Vibrational signals in the tremble dance of the honeybee, Apis mellifera. Behav Ecol Sociobiol 33:169–172

    Google Scholar 

  • Laidlaw HH Jr, Page RE Jr (1997) Queen rearing and bee breeding. Wicwas, Cheshire, Conn.

  • Makarov YI (1969) Biologically and economically useful characters of far eastern bees and their selection. PhD thesis, Timiryazev Academy of Agriculture, Moscow

  • 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 128:263–272

    Google Scholar 

  • Michener C, D, (1974) The social behavior of the bees. Harvard University Press, Cambridge, Mass.

  • Mohammedi A, Le Conte Y (2000) Do environmental conditions exert an effect on nest-mate recognition in queen rearing honey bees? Insectes Soc 47:307–312

    Google Scholar 

  • Moritz RFA (1985) The effects of multiple mating on the worker-queen conflict in Apis mellifera. Behav Ecol Sociobiol 16:1986

    Google Scholar 

  • Noonan KC (1986) Recognition of queen larvae by worker honey bees (Apis mellifera). Ethology 73:295–306

    Google Scholar 

  • 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 91:700–709

    CAS  Google Scholar 

  • Oldroyd BP, Rinderer TE, Buco SM (1990) Nepotism in the honey bee. Nature 346:707–708

    Article  Google Scholar 

  • Osborne KE, Oldroyd BP (1999) Possible causes of reproductive dominance during emergency queen rearing by honeybees. Anim Behav 58:267–272

    Article  PubMed  Google Scholar 

  • Page RE Jr, Erickson EH (1984) Selective queen rearing by worker honeybees: kin or nestmate recognition. Ann Entomol Soc Am 77:578–580

    Google Scholar 

  • Page RE Jr, Erickson EH Jr (1986a) Kin recognition during emergency queen rearing by worker honey bees (Hymenoptera: Apidae). Ann Entomol Soc Am 79:460–467

    Google Scholar 

  • Page RE Jr, Erickson EH (1986b) Kin recognition of virgin queen acceptance by worker honey bees (Apis mellifera L.). Anim Behav 34:1061–1069

    Google Scholar 

  • Page RE Jr, Peng CYS (2001) Aging and development in social insects with emphasis on the honey bee, Apis mellifera L. Exp Gerontol 36:695–711

    PubMed  Google Scholar 

  • Page RE Jr, Blum MS, Fales HM (1988) o-Aminoacetophenone, a pheromone that repels honeybees (Apis mellifera L.). Experientia 44:270–271

    CAS  PubMed  Google Scholar 

  • Page RE Jr, Robinson GE, Fondrk MK (1989) Genetic specialists, kin recognition and nepotism in honeybee colonies. Nature 339:576–579

    Article  Google Scholar 

  • Pankiw T (1997) Queen rearing by high and low queen mandibular pheromone responding worker honey bees (Apis mellifera L.). Can Entomol 129:679–690

    Google Scholar 

  • 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 13:583–591

    Google Scholar 

  • Queller DC, Strassmann JE (2002) The many selves of social insects. Science 296:311–313

    Article  CAS  PubMed  Google Scholar 

  • Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial hymenoptera. Am Nat 132:217–236

    Article  Google Scholar 

  • Ratnieks FLW (1989) Conflict and cooperation in insect societies. PhD thesis, Cornell University, Ithaca, N.Y.

  • 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 158:33–65

    Google Scholar 

  • Robinson GE, Page RE, Jr., Arensen N (1994) Genotypic differences in brood rearing in honey bee colonies: context-specific? Behav Ecol Sociobiol 34:125–137

    Article  Google Scholar 

  • 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 51:415–425

    Article  Google Scholar 

  • Schneider SS, DeGrandi-Hoffman G (2002) The influence of worker behavior and paternity on the development and emergence of honey bee queens. Insectes Soc 49:306–314

    Google Scholar 

  • Schneider SS, DeGrandi-Hoffman G (2003) The influence of paternity on virgin queen success in hybrid colonies of European and African honeybees. Anim Behav 65:883–892

    Article  Google Scholar 

  • 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 61:1173–1180

    Article  Google Scholar 

  • Sundström L, Boomsma JJ (2001) Conflicts and alliances in insect families. Heredity 86:515–521

    Article  PubMed  Google Scholar 

  • Tarpy DR, Fletcher DJC (1998) Effects of relatedness on queen competition within honey bee colonies. Anim Behav 55:537–543

    Article  PubMed  Google Scholar 

  • Tarpy DR, Fletcher DJC (2003) ‘Spraying’ behavior during queen competition in honey bees. J Insect Behav 16:425–437

    Article  Google Scholar 

  • Tarpy DR, Nielsen DI (2002) Sampling error, effective paternity, and estimating the genetic structure of honey bee colonies (Hymenoptera:Apidae). Ann Entomol Soc Am 95:513–528

    Google Scholar 

  • Tarpy DR, Hatch S, Fletcher DJC (2000) The influence of queen age and quality during queen replacement in honeybee colonies. Anim Behav 59:97–101

    Article  PubMed  Google Scholar 

  • Tilley CA, Oldroyd BP (1997) Unequal subfamily proportions among honey bee queen and worker brood. Anim Behav 54:1483–1490

    Article  PubMed  Google Scholar 

  • Visscher PK (1986) Kinship discrimination in queen rearing by honey bees (Apis mellifera). Behav Ecol Sociobiol 18:453–460

    Google Scholar 

  • Visscher PK (1993) A theoretical analysis of individual interests and intracolony conflict during swarming of honey bee colonies. J Theor Biol 165:191–212

    Article  Google Scholar 

  • Visscher PK (1998) Colony integration and reproductive conflict in honey bees. Apidologie 29:23–45

    Google Scholar 

  • Wilson DS (1997) Multilevel selection theory comes of age—introduction. Am Nat 150:S1–S4

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard University Press, Cambridge, Mass.

  • Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge, Mass.

  • Winston ML, Taylor OR (1980) Factors preceding queen rearing in the Africanized honeybee (Apis melifera) in South America. Insectes Soc 27:289–304

    Google Scholar 

  • Woyciechowski M (1990) Do honey bee, Apis mellifera L., workers favour sibling eggs and larvae in queen rearing? Anim Behav 39:1220–1222

    Google Scholar 

  • Woyciechowski M, Lomnicki A (1987) Multiple mating of queens and the sterility of workers among eusocial Hymenoptera. J Theor Biol 128:317–328

    Google Scholar 

  • 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 10:45–55

    Google Scholar 

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Acknowledgements

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.

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Authors and Affiliations

  1. Department of Entomology, North Carolina State University, Campus Box 7613, Raleigh, NC 27695–7613, USA

    David R. Tarpy

  2. Carl Hayden Bee Research Center, 2000 East Allen Rd., Tucson, AZ 85719–1596, USA

    David C. Gilley

  3. Department of Neurobiology and Behavior, Cornell University, Seeley G. Mudd Hall, Ithaca, NY 14853, USA

    Thomas D. Seeley

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  1. David R. Tarpy
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  2. David C. Gilley
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  3. Thomas D. Seeley
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Correspondence to David R. Tarpy.

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Communicated by A. Cockburn

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Tarpy, D.R., Gilley, D.C. & Seeley, T.D. Levels of selection in a social insect: a review of conflict and cooperation during honey bee (Apis mellifera) queen replacement. Behav Ecol Sociobiol 55, 513–523 (2004). https://doi.org/10.1007/s00265-003-0738-5

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