Behavioral Ecology and Sociobiology

, Volume 64, Issue 5, pp 875–889 | Cite as

Promiscuous honeybee queens generate colonies with a critical minority of waggle-dancing foragers

  • Heather R. MattilaEmail author
  • Thomas D. Seeley
Original Paper


Honeybees present a paradox that is unusual among the social Hymenoptera: extremely promiscuous queens generate colonies of nonreproducing workers who cooperate to rear reproductives with whom they share limited kinship. Extreme polyandry, which lowers relatedness but creates within-colony genetic diversity, produces substantial fitness benefits for honeybee queens and their colonies because of increased disease resistance and workforce productivity. However, the way that these increases are generated by individuals in genetically diverse colonies remains a mystery. We assayed the foraging and dancing performances of workers in multiple-patriline and single-patriline colonies to discover how within-colony genetic diversity, conferred to colonies by polyandrous queens, gives rise to a more productive foraging effort. We also determined whether the initiation by foragers of waggle-dance signaling in response to an increasing sucrose stimulus (their dance response thresholds) was linked to patriline membership. Per capita, foragers in multiple-patriline colonies visited a food source more often and advertised it with more waggle-dance signals than foragers from single-patriline colonies, although there was variability among multiple-patriline colonies in the strength of this difference. High-participation patrilines emerged within multiple-patriline colonies, but their more numerous foragers and dancers were neither more active per capita nor lower-threshold dancers than their counterparts from low-participation patrilines. Our results demonstrate that extreme polyandry does not enhance recruitment effort through the introduction of low-dance-threshold, high-activity workers into a colony’s population. Rather, genetic diversity is critical for injecting into a colony’s workforce social facilitators who are more likely to become engaged in foraging-related activities, so boosting the production of dance signals and a colony’s responsiveness to profitable food sources.


Intracolonial genetic diversity Polyandry Recruitment signaling Response thresholds Task allocation Waggle-dance communication 



We are grateful to M. Girard for dedicated assistance in the field and with sample processing. We also thank S. Bogdanowicz and M. Jandricic for assistance with genotyping. We appreciate stimulating feedback from A. Weidenmüller on an early version of the manuscript and careful review of the submitted draft from three reviewers. This project was funded by a Natural Sciences and Engineering Research Council of Canada Postdoctoral Fellowship (H.R.M.) and two Cooperative State Research, Education, and Extension Service National Research Initiative grants (T.D.S.: 2003-35302-13387 and 2007-35302-18174).

Conflict of interest statement

The authors declare that they have no conflict of interest.


  1. Arnold G, Quenet B, Papin C, Masson C, Kirchner WH (2002) Intra-colonial variability in the dance communication in honeybees (Apis mellifera). Ethology 108:751–761CrossRefGoogle Scholar
  2. Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440CrossRefPubMedGoogle Scholar
  3. Bonabeau E, Theraulaz G, Deneubourg JL (1998) Fixed response thresholds and the regulation of division of labor in insect societies. B Math Biol 60:753–807CrossRefGoogle Scholar
  4. Boomsma JJ, Fjerdingstad EJ, Frydenberg J (1999) Multiple paternity, relatedness and genetic diversity in Acromyrmex leaf-cutter ants. Proc R Soc London B 266:249–254CrossRefGoogle Scholar
  5. Cole BJ, Wiernasz DC (1999) The selective advantage of low relatedness. Science 285:891–893CrossRefPubMedGoogle Scholar
  6. Denny AJ, Franks NR, Powell S, Edwards KJ (2004) Exceptionally high levels of multiple mating in an army ant. Naturwiss 91:396–399CrossRefPubMedGoogle Scholar
  7. Fjerdingstad EJ, Boomsma JJ (2000) Queen mating frequency and relatedness in young Atta sexdens colonies. Insectes Soc 47:354–356CrossRefGoogle Scholar
  8. Fjerdingstad EF, Boomsma JJ, Thoren P (1998) Multiple paternity in the leafcutter ant Atta colombica, a microsatellite DNA study. Heredity 80:118–126CrossRefGoogle Scholar
  9. Gadau J, Strehl CP, Oettler J, Hölldobler B (2003) Determinants of intracolonial relatedness in Pogonomyrmex rugosus (Hymenoptera; Formicidae): mating frequency and brood raids. Mol Ecol 12:1931–1938CrossRefPubMedGoogle Scholar
  10. Gardner KE, Seeley TD, Calderone NW (2008) Do honeybees have two discrete dances to advertise food sources? Anim Behav 75:1291–1300CrossRefGoogle Scholar
  11. Goodisman MAD, Kovacs JL, Hoffman EA (2007) The significance of multiple mating in the social wasp Vespula maculifrons. Evolution 61:2260–2267CrossRefPubMedGoogle Scholar
  12. Hamilton WD (1964) The genetical evolution of social behaviour I and II. J Theor Biol 7(1–16):17–52CrossRefPubMedGoogle Scholar
  13. Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58:1251–1260PubMedGoogle Scholar
  14. Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213–1216CrossRefPubMedGoogle Scholar
  15. Jeanson R, Fewell JH, Gorelick R (2007) Emergence of increased division of labor as a function of group size. Behav Ecol Sociobiol 62:289–298CrossRefGoogle Scholar
  16. Jones JC, Myerscough MR, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404CrossRefPubMedGoogle Scholar
  17. Kronauer DJC, Schöning C, Pedersen JS, Boomsma JJ, Gadau J (2004) Extreme queen-mating frequency and colony fission in African army ants. Mol Ecol 13:2381–2388CrossRefPubMedGoogle Scholar
  18. Kronauer DJC, Johnson RA, Boomsma JJ (2007) The evolution of multiple mating in army ants. Evolution 61:413–422CrossRefPubMedGoogle Scholar
  19. Mailleux AC, Deneubourg JL, Detrain C (2000) How do ants assess food volume? Anim Behav 59:1061–1069CrossRefPubMedGoogle Scholar
  20. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364CrossRefPubMedGoogle Scholar
  21. Mattila HR, Burke KM, Seeley TD (2008) Genetic diversity within honeybee colonies increases signal production by waggle-dancing foragers. Proc R Soc London B 275:809–816CrossRefGoogle Scholar
  22. O’Donnell S, Foster RL (2001) Thresholds of response in nest thermoregulation by worker bumble bees, Bombus bifarius nearcticus (Hymenoptera: Apidae). Ethology 107:387–399CrossRefGoogle Scholar
  23. Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect societies. Trends Ecol Evol 22:408–413CrossRefPubMedGoogle Scholar
  24. Page RE, Erber J, Fondrk MK (1998) The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 182:489–500CrossRefPubMedGoogle Scholar
  25. Pol RG, Lopez de Casenave J, Feldhaar H, Milesi FA, Gadau J (2008) Polyandry in two South American harvester ants. Insectes Soc 55:91–97CrossRefGoogle Scholar
  26. Rheindt FE, Gadau J, Strehl CP, Hölldobler B (2004) Extremely high mating frequency in the Florida harvester ant (Pogonomyrmex badius). Behav Ecol Sociobiol 56:472–481CrossRefGoogle Scholar
  27. Robinson GE, Page RE (1989) Genetic basis for division of labor in an insect society. In: Breed MD, Page RE (eds) The genetics of social evolution. Westview, Boulder, pp 61–68Google Scholar
  28. Ross KG (1986) Kin selection and the problem of sperm utilization in social insects. Nature 323:798–800CrossRefGoogle Scholar
  29. Seeley TD (1995) The wisdom of the hive. Harvard University Press, CambridgeGoogle Scholar
  30. Seeley TD, Tarpy DR (2007) Queen promiscuity lowers disease within honeybee colonies. Proc R Soc London B 274:67–72CrossRefGoogle Scholar
  31. Solignac M, Vautrin D, Loiseau A, Mougel F, Baudry E, Estoup A, Garnery L, Haberl M, Cornuet JM (2003) Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Mol Ecol Notes 3:307–311CrossRefGoogle Scholar
  32. Strassmann J (2001) The rarity of multiple mating by females in the social Hymenoptera. Insectes Soc 48:1–13CrossRefGoogle Scholar
  33. Tarpy DR, Nielsen DI (2002) Sampling error, effective paternity, and estimating the genetic structure of honey bee colonies (Hymenoptera: Apidae). Ann Entomol Soc Am 95:513–528CrossRefGoogle Scholar
  34. Tarpy DR, Page RE (2002) Sex determination and the evolution of polyandry in honey bees (Apis mellifera). Behav Ecol Sociobiol 52:143–150CrossRefGoogle Scholar
  35. Tarpy DR, Nielsen R, Nielsen DI (2004) A scientific note on the revised estimates of effective paternity frequency in Apis. Insectes Soc 51:203–204CrossRefGoogle Scholar
  36. Timmermans I, Hefetz A, Fournier D, Aron S (2008) Population genetic structure, worker reproduction and thelytokous parthenogenesis in the desert ant Cataglyphis sabulosa. Heredity 101:490–498CrossRefPubMedGoogle Scholar
  37. van Wilgenburg E, Driessen G, Beukeboom LW (2006) Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Front Zool 3:1–15CrossRefPubMedGoogle Scholar
  38. Waibel M, Floreano D, Magnenat S, Keller L (2006) Division of labour and colony efficiency in social insects: effects of interactions between genetic architecture, colony kin structure and rate of perturbations. Proc R Soc London B 273:1815–1823CrossRefGoogle Scholar
  39. Weidenmüller A (2003) The control of nest climate in bumblebee (Bombus terrestris) colonies: interindividual variability and self reinforcement in fanning response. Behav Ecol 15:120–128CrossRefGoogle Scholar
  40. Wiernasz DC, Perroni CL, Cole BJ (2004) Polyandry and fitness in the western harvester ant, Pogonomyrmex occidentalis. Mol Ecol 13:1601–1606CrossRefPubMedGoogle Scholar
  41. Wiernasz DC, Hines J, Parker DG, Cole BJ (2008) Mating for variety increases foraging activity in the harvester ant, Pogonomyrmex occidentalis. Mol Ecol 17:1137–1144CrossRefPubMedGoogle Scholar
  42. Wilson EO (1971) The insect societies. Belknap, CambridgeGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of Neurobiology and BehaviorCornell UniversityIthacaUSA
  2. 2.Department of Biological SciencesWellesley CollegeWellesleyUSA

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