Advertisement

Insectes Sociaux

, Volume 56, Issue 3, pp 319–331 | Cite as

Division of labour and social insect colony performance in relation to task and mating number under two alternative response threshold models

  • R. Gove
  • M. Hayworth
  • M. Chhetri
  • O. Rueppell
Research Article

Abstract

Some social insects exhibit an exceptionally high degree of polyandry. Alternative hypotheses exist to explain the benefits of multiple mating through enhanced colony performance. This study critically extends theoretical analyses of the hypothesis that enhanced division of labour confers fitness benefits to the queen that are sufficient to explain the observed mating frequencies of social insects. The effects of widely varying numbers of tasks and matings were systematically investigated in two alternative computer simulation models. One model was based on tasks that have to be performed to maintain an optimal trait value, while the other model was based on tasks that only have to be sufficiently performed to exceed a minimum trait value to confer full fitness returns. Both model versions were evaluated assuming a broad and a narrow response threshold distribution. The results consistently suggest a beneficial effect of multiple mating on colony performance, albeit with quickly diminishing returns. An increasing number of tasks decreased performance of colonies with few patrilines but not of more genetically diverse colonies. Instead, a performance maximum was found for intermediate task numbers. The results from the two model versions and two response threshold distributions did not fundamentally differ, suggesting that the type of tasks and the breadth of response thresholds do not affect the benefit of multiple mating. In general, our results corroborate previous models that have evaluated simpler task/patriline scenarios. Furthermore, selection for an intermediate number of tasks is indicated that could constrain the degree of division of labour. We conclude that enhanced division of labour may have favoured the evolution of multiple mating but is insufficient to explain the extreme mating numbers observed in some social insects, even in complex task scenarios.

Keywords

Multiple mating Social evolution Division of labour Genetic variability Colony efficiency Computer simulations 

Notes

Acknowledgments

We would like to thank all members of the UNCG Math-Bio group for their comments, suggestions, and lively discussion. This study was improved by the comments of two anonymous reviewers of an earlier version of this manuscript but potential errors remain our own. Financial support was provided by NSF (#0634182 and #0615502). The work performed adheres to all applicable ethical standards and government regulations.

References

  1. Baer B. and Schmid-Hempel P. 1999. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397: 151-154CrossRefGoogle Scholar
  2. Bastian J. and Esch H. 1970. The nervous control of the indirect flight muscles of the honey bee. Z. vergl. Physiol. 67: 307-324CrossRefGoogle Scholar
  3. Beekman M., Sumpter, D.J.T. and Ratnieks, F.L.W. 2001. Phase transition between disordered and ordered foraging in Pharaoh’s ants. Proc. Natl Acad. Sci. 98: 9703-9706PubMedCrossRefGoogle Scholar
  4. Bertram S.M., Gorelick R. and Fewell J.H. 2003. Colony response to graded resource changes: an analytical model of the influence of genotype, environment, and dominance. Theor. Pop. Biol. 64: 151-162CrossRefGoogle Scholar
  5. Beshers S.N. and Fewell J.H. 2001. Models of division of labor in social insects. Annu. Rev. Entomol. 46: 413-440PubMedCrossRefGoogle Scholar
  6. Beye M., Gattermeier I., Hasselmann M., Gempe T., Schioett M., Baines J.F., Schlipalius D., Mougel F., Emore C., Rueppell O., Sirvio A., Guzman-Novoa E., Hunt G., Solignac M. and Page R.E. 2006. Exceptionally high levels of recombination across the honey bee genome. Genome Res. 16: 1339-1344PubMedCrossRefGoogle Scholar
  7. Breed M.D., Robinson G.E. and Page R.E. 1990. Division of labor during honey bee colony defense. Behav. Ecol. Sociobiol. 27: 395-401CrossRefGoogle Scholar
  8. Brown M.J.F. and Schmid-Hempel P. 2003. The evolution of female multiple mating in social Hymenoptera. Evolution 57: 2067-2081PubMedGoogle Scholar
  9. Camazine S. 1993. The regulation of pollen foraging by honey bees: How foragers assess the colony’s need for pollen. Behav. Ecol. Sociobiol. 32: 265-273CrossRefGoogle Scholar
  10. Chadwick P. 1931. Ventilation of the hive. Glean. Bee Cult. 59: 356-358Google Scholar
  11. Chapman N.C., Oldroyd B.P. and Hughes W.O.H. 2007. Differential responses of honeybee (Apis mellifera) patrilines to changes in stimuli for the generalist tasks of nursing and foraging. Behav. Ecol. Sociobiol. 61: 1185-1194CrossRefGoogle Scholar
  12. Crozier R.H. and Consul P.C. 1976. Conditions for genetic polymorphism in social hymenoptera under selection at the colony level. Theor. Popul. Biol. 10:1-9PubMedCrossRefGoogle Scholar
  13. Crozier R.H. and Page R.E. 1985. On being the right size: male contributions and multiple mating in social Hymenoptera. Behav. Ecol. Sociobiol. 18: 105-115CrossRefGoogle Scholar
  14. Dreller C. and Tarpy D.R. 2000. Perception of the pollen need by foragers in a honeybee colony. Anim. Behav. 59: 91–96PubMedCrossRefGoogle Scholar
  15. Fewell J.H. and Page R.E. 1993. Genotypic variation in foraging responses to environmental stimuli by honey-bees, Apis mellifera. Experientia 49: 1106-1112CrossRefGoogle Scholar
  16. Fewell J.H. and Winston M.L. 1992. Colony state and regulation of pollen foraging in the honey-bee, Apis mellifera L. Behav. Ecol. Sociobiol. 30: 387-393CrossRefGoogle Scholar
  17. Fjerdingstad E.J. and Boomsma, J.J. 2000. Queen mating frequency and relatedness in young Atta sexdens colonies. Insect. Soc. 47: 354-356CrossRefGoogle Scholar
  18. Fournier D., Battaille G., Timmermans I. and Aron S. 2008. Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor. Anim. Behav. 75: 151-158CrossRefGoogle Scholar
  19. Fuchs S. and Moritz R.F.A. 1999. Evolution of extreme polyandry in the honeybee Apis mellifera L. Behav. Ecol. Sociobiol. 45: 269-275CrossRefGoogle Scholar
  20. Fuchs S. and Schade V. 1994. Lower performance in honeybee colonies of uniform paternity. Apidologie 25: 155-169CrossRefGoogle Scholar
  21. Goode K., Huber Z., Mesce K.A. and Spivak M. 2006. Hygienic behavior of the honey bee (Apis mellifera) is independent of sucrose responsiveness and foraging ontogeny. Horm. Behav. 49: 391-397PubMedCrossRefGoogle Scholar
  22. Graham S., Myerscough M.R., Jones J.C. and Oldroyd B.P. 2006. Modelling the role of intracolonial genetic diversity on regulation of brood temperature in honey bee (Apis mellifera L.) colonies. Insect. Soc. 53: 226-232CrossRefGoogle Scholar
  23. Hölldobler B. and Wilson E.O. 1990. The Ants. The Belknap Press of Harvard University Press, Cambridge. 732 ppGoogle Scholar
  24. Hughes W.O.H. and Boomsma J.J. 2004. Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58: 1251-1260PubMedGoogle Scholar
  25. Hughes W.O.H. and Boomsma J.J. 2007. Genetic polymorphism in leaf-cutting ants is phenotypically plastic. Proc. R. Soc. Lond. B. 274: 1625-1630CrossRefGoogle Scholar
  26. Jaffe R., Kronauer D.J.C., Kraus F.B., Boomsma J.J. and Moritz R.F.A. 2007. Worker caste determination in the army ant Eciton burchellii. Biol. Lett. 3: 513-516PubMedCrossRefGoogle Scholar
  27. Jeanson R., Fewell J.H., Gorelick R. and Bertram S.M. 2007. Emergence of increased division of labor as a function of group size. Behav. Ecol. Sociobiol. 62: 289-298CrossRefGoogle Scholar
  28. Johnson B.R. 2008a. Within-nest temporal polyethism in the honey bee. Behav. Ecol. Sociobiol. 62: 777-784CrossRefGoogle Scholar
  29. Johnson B.R. 2008b. Global information sampling in the honey bee. Naturwissenschaften 95: 523-530PubMedCrossRefGoogle Scholar
  30. Jones J.C., Myerscough M.R., Graham S. and Oldroyd B.P. 2004. Honey bee nest thermoregulation: Diversity promotes stability. Science 305: 402-404PubMedCrossRefGoogle Scholar
  31. Jones J.C., Nanork P. and Oldroyd B.P. 2007. The role of genetic diversity in nest cooling in a wild honey bee, Apis florea. J. Comp. Physiol. A. 193: 159-165.CrossRefGoogle Scholar
  32. Kallenberg O. 1997. Foundations of Modern Probability. Springer-Verlag, New York. 515 ppGoogle Scholar
  33. Kolmes S.A. 1985. A quantitative study of the division of labour among worker honeybees. Z. Tierpsychol. 68: 287-302Google Scholar
  34. Kronauer D.J.C., Johnson R.A. and Boomsma J.J. 2007. The evolution of multiple mating in army ants. Evolution 61: 413-422PubMedCrossRefGoogle Scholar
  35. Kryger P., Kryger U. and Moritz R.F.A. 2000. Genotypical variability for the tasks of water collecting and scenting in a honey bee colony. Ethology 106: 769-779CrossRefGoogle Scholar
  36. Lindauer M. 1952. Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat. Z. vergl. Physiol. 34: 299-345CrossRefGoogle Scholar
  37. Lindauer M. 1954. Temperaturregulierung und Wasserhaushalt im Bienenstaat. Z. vergl. Physiol. 36: 391-432CrossRefGoogle Scholar
  38. Mattila H.R., Burke K.M. and Seeley T.D. 2008. Genetic diversity within honeybee colonies increases signal production by waggle-dancing foragers. Proc. R. Soc. Lond. B. 275: 809-816CrossRefGoogle Scholar
  39. Mattila H.R. and Seeley T.D. 2007. Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317: 362-364PubMedCrossRefGoogle Scholar
  40. Maynard Smith J. and Szathmáry E. 1995. The Major Transitions in Evolution. W.H. Freeman, San Francisco. 360 ppGoogle Scholar
  41. Moritz R.F.A. 1985. The effect of multiple mating on the worker-queen conflict in Apis mellifera. Behav. Ecol. Sociobiol. 16: 375-377CrossRefGoogle Scholar
  42. Myerscough M.R. and Oldroyd B.P. 2004. Simulation models of the role of genetic variability in social insect task allocation. Insect. Soc. 51: 146-152CrossRefGoogle Scholar
  43. Oldroyd B.P. and Fewell J.H. 2007. Genetic diversity promotes homeostasis in insect colonies. Trend Ecol. Evol. 22: 408-413CrossRefGoogle Scholar
  44. Oldroyd B.P., Sylvester H.A., Wongsiri S. and Rinderer T.E. 1994. Task specialization in a wild-bee, Apis florea (Hymenoptera, Apidae), revealed by RFLP banding. Behav. Ecol. Sociobiol. 34: 25-30CrossRefGoogle Scholar
  45. Oster G.F. and Wilson E.O. 1978. Caste and Ecology in the Social Insects. Princeton University Press, Princeton. 352 ppGoogle Scholar
  46. Page R.E. 1980. The evolution of multiple mating behavior by honey bee queens Apis mellifera L. Genetics 96: 263-273PubMedGoogle Scholar
  47. Page R.E. and Fondrk M.K. 1995. The effects of colony level selection on the social-organization of honey-bee (Apis mellifera L) colonies-colony level components of pollen hoarding. Behav. Ecol. Sociobiol. 36: 135-144CrossRefGoogle Scholar
  48. Page R.E. and Mitchell S.D. 1998. Self-organization and the evolution of division of labor. Apidologie 29: 171-190CrossRefGoogle Scholar
  49. Page R.E., Robinson G.E., Fondrk M.K. and Nasr M.R. 1995. Effects of worker genotypic diversity on honey-bee colony development and behaviour (Apis mellifera L). Behav. Ecol. Sociobiol. 36: 387-396CrossRefGoogle Scholar
  50. Pankiw T. 2004a. Brood pheromone regulates foraging activity of honey bees (Hymenoptera: Apidae). J. Econ. Entomol. 97: 748–751PubMedCrossRefGoogle Scholar
  51. Pankiw T. 2004b. Cued in: Honey bee pheromones as information flow and colony decision making. Apidologie 35: 217–226CrossRefGoogle Scholar
  52. Pankiw T. 2007. Brood pheromone modulation of pollen forager turnaround time in the honey bee (Apis mellifera L.). J. Insect Behav. 20: 173-180CrossRefGoogle Scholar
  53. Pankiw T. and Page R.E. 1999. The effects of genotype, age, and caste on response thresholds to sucrose and foraging behavior of honey bees. J. Comp. Physiol. A. 185: 207-213PubMedCrossRefGoogle Scholar
  54. Pankiw T. and Page R.E. 2001. Brood pheromone modulates sucrose response thresholds in honeybees (Apis mellifera L.). Behav. Ecol. Sociobiol. 49: 206–213CrossRefGoogle Scholar
  55. Pankiw T., Page R.E. and Fondrk M.K. 1998. Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera). Behav. Ecol. Sociobiol. 44: 193–198CrossRefGoogle Scholar
  56. Pankiw T. and Rubink W.L. 2002. Pollen foraging response to brood pheromone by Africanized and European honey bees (Apis mellifera L.). Ann. Entomol. Soc. Am. 95: 761–767CrossRefGoogle Scholar
  57. Pankiw T., Tarpy D.R. and Page R.E. 2002. Genotype and rearing environment affect honeybee perception and foraging behaviour. Anim. Behav. 64: 663-672CrossRefGoogle Scholar
  58. Ratnieks F.L.W. and Boomsma J.J. 1995. Facultative sex allocation by workers and the evolution of polyandry by queens in social Hymenoptera. Am. Nat. 145: 969-993CrossRefGoogle Scholar
  59. Robinson G.E. and Page R.E. 1988. Genetic determination of guarding and undertaking in honeybee colonies. Nature 333: 356-358CrossRefGoogle Scholar
  60. Robinson G.E. and Page R.E. 1989. Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behav. Ecol. Sociobiol. 24: 317-323CrossRefGoogle Scholar
  61. Robinson G.E. and Page R.E. 1995. Genotypic constraints on plasticity for corpse removal in honey-bee colonies. Anim. Behav. 49: 867-876.CrossRefGoogle Scholar
  62. Rueppell O., Johnson N. and Rychtár J. 2008. Variance-based selection may explain general mating patterns in social insects. Biol. Lett. 4: 270-273PubMedCrossRefGoogle Scholar
  63. Schmid-Hempel P. 1998. Parasites in Social Insects. Princeton University Press, Princeton. 392 ppGoogle Scholar
  64. Schneider S.S. 1987. The modulation of worker activity by the vibration dance of the honeybee Apis mellifera. Ethology 74: 211-218CrossRefGoogle Scholar
  65. Schneider S.S., Stamps J.A. and Gary N.E. 1986. The vibration dance of the honey bee. I. Communication regulating foraging on two time scales. Anim. Behav. 34: 366-85Google Scholar
  66. Seeley T.D. and Tarpy D.R. 2007. Queen promiscuity lowers disease within honeybee colonies. Proc. R. Soc. Lond. B. 274: 67-72CrossRefGoogle Scholar
  67. Sherman P.W., Seeley T.D. and Hudson K.R. 1988. Parasites, pathogens, and polyandry in social Hymenoptera. Am. Nat. 131: 602-610CrossRefGoogle Scholar
  68. Shykoff J.A. and Schmid-Hempel P. 1991. Parasites and the advantage of genetic variability within social insect colonies. Proc. R. Soc. Lond. B. 243: 55–58CrossRefGoogle Scholar
  69. Tarpy D.R. and Page R.E. 2001. The curious promiscuity of queen honey bees (Apis mellifera): evolutionary and behavioral mechanisms. Ann. Zool. Fenn. 38: 255-265Google Scholar
  70. Tofts C. and Franks N.R. 1992. Doing the right thing - Ants, honeybees and naked mole-rats. Trends Ecol. Evol. 7: 346-349CrossRefGoogle Scholar
  71. van Baalen M. and Beekman M. 2006. The costs and benefits of genetic heterogeneity in resistance against parasites in social insects. Am. Nat. 167: 568-577PubMedCrossRefGoogle Scholar
  72. Waibel M., Floreano D., Magnenat S. and 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. B. 273: 1815-1823PubMedCrossRefGoogle Scholar
  73. Wattanachaiyingcharoen W., Oldroyd B.P., Wongsiri S., Palmer K. and Paar R. 2003. A scientific note on the mating frequency of Apis dorsata. Apidologie 34: 85-86CrossRefGoogle Scholar
  74. Weidenmuller A. 2004. The control of nest climate in bumblebee (Bombus terrestris) colonies: interindividual variability and self reinforcement in fanning response. Behav. Ecol. 15: 120-128CrossRefGoogle Scholar
  75. Wiernasz D.C., Hines J., Parker D.G. and Cole B.J. 2008. Mating for variety increases foraging activity in the harvester ant, Pogonomyrmex occidentalis. Mol. Ecol. 17: 1137-1144PubMedCrossRefGoogle Scholar
  76. Wiernasz D.C., Perroni D.L. and Cole B.J. 2004. Polyandry and fitness in the western harvester ant, Pogonomyrmex occidentalis. Mol. Ecol. 13: 1601-1606PubMedCrossRefGoogle Scholar
  77. Wilfert L., Gadau J. and Schmid-Hempel P. 2007. Variation in genomic recombination rates among animal taxa and the case of social insects. Heredity 98: 189-197PubMedCrossRefGoogle Scholar
  78. Wilson E.O. 1976. Behavioral discretization and the number of castes in an ant species. Behav. Ecol. Sociobiol. 1: 141-154CrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  • R. Gove
    • 1
  • M. Hayworth
    • 2
  • M. Chhetri
    • 1
  • O. Rueppell
    • 2
    • 3
  1. 1.Department of Mathematics and StatisticsUniversity of North CarolinaGreensboroUSA
  2. 2.Department of BiologyUniversity of North CarolinaGreensboroUSA
  3. 3.GreensboroUSA

Personalised recommendations