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Insectes Sociaux

, Volume 56, Issue 2, pp 119–129 | Cite as

Workers, sexuals, or both? Optimal allocation of resources to reproduction and growth in annual insect colonies

  • K. PoitrineauEmail author
  • O. Mitesser
  • H. J. Poethke
Research Article

Abstract

Understanding decisions about the allocation of resources into colony growth and reproduction in social insects is one of the challenging issues in sociobiology. In their seminal paper, Macevicz and Oster predicted that, for most annual insect colonies, a bang–bang strategy should be favoured by selection, i.e. a strategy characterised by an “ergonomic phase” with exponential colony growth followed by a “reproductive phase” with all resources invested into the production of sexuals. Yet, there is empirical evidence for the simultaneous investment into the production of workers and sexuals in annual colonies (graded control). We, therefore, re-analyse and extend the original model of Macevicz and Oster. Using basic calculus, we can show that sufficiently strong negative correlation between colony size and worker efficiency or increasing mortality of workers with increasing colony size will favour the evolution of graded allocation strategies. By similar reasoning, graded control is predicted for other factors limiting colony productivity (for example, if queens’ egg laying capacity is limited).

Keywords

Resource allocation Social insects Colony life cycle Optimality model Dynamic programming 

Notes

Acknowledgments

We would like to thank Thomas Hovestadt and two anonymous reviewers for their helpful and valuable comments on earlier drafts of the manuscript, and Christian Hausler for help with the English language. This work was supported by the Deutsche Forschungsgemeinschaft (SFB 554, TP C6).

References

  1. Anderson C. and Ratnieks F.L.W. 1999. Task partitioning in insect societies. I. Effect of colony size on queueing delay and colony ergonomic efficiency. Am. Nat. 154: 521–535PubMedCrossRefGoogle Scholar
  2. Beekman M., Lingeman R., Kleijne F.M. and Sabelis M.W. 1998. Optimal timing of the production of sexuals in bumblebee colonies. Entomol. Exp. Appl. 88: 147–154CrossRefGoogle Scholar
  3. Billick I. 2001. Density dependence and colony growth in the ant species Formica neorufibarbis. J. Anim. Ecol. 2: 895–905CrossRefGoogle Scholar
  4. Bouwma A.M., Nordheim E.V. and Jeanne R.L. 2006. Per-capita productivity in a social wasp: no evidence for a negative effect of colony size. Insect. Soc. 53: 412–419CrossRefGoogle Scholar
  5. Bulmer M.G. 1981. Worker–queen conflict in annual social Hymenoptera. J. Theor. Biol. 93: 239–251CrossRefGoogle Scholar
  6. Cassill D. 2002. Yoyo-bang: a risk-aversion investment strategy by a perennial insect society. Oecologia 132: 150–158CrossRefGoogle Scholar
  7. Clouse R. 2001. Some effects of group size on the output of beginning nests of Mischocyttarus mexicanus (Hymenoptera: Vespidae). Florida Entomol. 84: 418–425CrossRefGoogle Scholar
  8. Gadagkar R. 1991. Demographic prediction to predisposition to the evolution of eusociality—a hierarchy of models. Proc. Natl. Acad. Sci. USA 88: 10993–10997PubMedCrossRefGoogle Scholar
  9. Greene A. 1984. Production schedules of vespine wasps—an empirical-test of the bang–bang optimization model. J. Kans. Entomol. Soc. 57: 545–568Google Scholar
  10. Hansell M. 1987. Nest building as a facilitating and limiting factor in the evolution of eusociality in the Hymenoptera. Oxf. Surv. Evol. Biol. 4: 155–181Google Scholar
  11. Hee J., Holway D., Suarez A. and Case T. 2000. Role of propagule size in the success of incipient colonies of the invasive argentine ant. Conserv. Biol. 14: 559–563CrossRefGoogle Scholar
  12. Heino M. and Kaitala V. 1999. Evolution of resource allocation between growth and reproduction in animals with indeterminate growth. J. Evol. Biol. 12: 423–429CrossRefGoogle Scholar
  13. Heinze J., Hölldobler B. and Peeters C. 1994. Conflict and cooperation in ant societies. Naturwissenschaften 81: 489–497CrossRefGoogle Scholar
  14. Houston A., Schmid-Hempel P. and Kacelnik A. 1988. Foraging strategy, worker mortality, and the growth of the colony in social insects. Am. Nat. 131: 107–114CrossRefGoogle Scholar
  15. Iwasa Y. 2000. Dynamic optimization of plant growth. Evol. Ecol. Res. 2: 437–455Google Scholar
  16. Jeanne R.L. 1986. The organization of work in Polybia occidentalis: costs and benefits of specialization in a social wasp. Behav. Ecol. Sociobiol. 19: 333–341CrossRefGoogle Scholar
  17. Jeanne R.L. and Nordheim E.V. 1996. Productivity in a social wasp: per capita output increases with swarm size. Behav. Ecol. 7: 43–48CrossRefGoogle Scholar
  18. Jun J., Pepper J.W., Savage V.M., Gillooly J.F. and Brown J.H. 2003. Allometric scaling of ant foraging trail networks. Evol. Ecol. Res. 5: 297–303Google Scholar
  19. Karsai I. and Wenzel J.W. 1998. Productivity, individual-level and colony-level flexibility, and organization of work as consequences of colony size. Proc. Natl. Acad. Sci. USA 95: 8665–8669PubMedCrossRefGoogle Scholar
  20. Kaspari M. and O’Donnell S. 2003. High rates of army ant raids in the neotropics and implications for ant colony and community structure. Evol. Ecol. Res. 5: 933–939Google Scholar
  21. Kikuta N. and Tsuji K. 1999. Queen and worker policing in the monogynous and monandrous ant, Diacamma sp. Behav. Ecol. Sociobiol. 46: 180–189CrossRefGoogle Scholar
  22. King D. and Roughgarden J. 1982a. Multiple switches between vegetative and reproductive growth in annual plants. Theor. Popul. Biol. 21: 194–204CrossRefGoogle Scholar
  23. King D. and Roughgarden J. 1982b. Graded allocation between vegetative and reproductive growth for annual plants in growing seasons of random length. Theor. Popul. Biol. 22: 1–16CrossRefGoogle Scholar
  24. King D. and Roughgarden J. 1983. Energy allocation patterns of the California grassland annuals Plantago erecta and Clarkia rubicunda. Ecology 64: 16–24CrossRefGoogle Scholar
  25. Kozlowski J. and Wiegert R.G. 1987. Optimal age and size at maturity in annuals and perennials with determinate growth. Evol. Ecol. 1: 231–244CrossRefGoogle Scholar
  26. Lika K. and Nisbet R.M. 2000. A dynamic energy budget model based on partitioning of net production. J. Math. Biol. 41: 361–386PubMedCrossRefGoogle Scholar
  27. Macevicz S. and Oster G. 1976. Modeling social insect populations. 2. Optimal reproductive strategies in annual eusocial insect colonies. Behav. Ecol. Sociobiol. 1: 265–282CrossRefGoogle Scholar
  28. Mangel M. and Clark C.W. 1988 Dynamic Modeling in Behavioral Ecology. Princeton University Press, Princeton. 320 ppGoogle Scholar
  29. McCauley E., Murdoch W.W., Nisbet R.M. and Gurney W.S.C. 1990. The physiological ecology of Daphnia: development of a model of growth and reproduction. Ecology 71: 703–715CrossRefGoogle Scholar
  30. Michener C.D. 1964. Reproductive efficiency in relation to colony size in hymenopterous societies. Insect. Soc. 11: 317–342CrossRefGoogle Scholar
  31. Mitesser O., Weissel N., Strohm E. and Poethke H.J. 2007. Adaptive dynamic resource allocation in annual eusocial insects: environmental variation will not necessarily promote graded control. BMC Ecol. 7: 16PubMedCrossRefGoogle Scholar
  32. Mitesser O., Weissel N., Strohm E. and Poethke H.J. 2007. Optimal investment allocation in primitively eusocial bees: a balance model based on resource limitation of the queen. Insect. Soc. 54: 234–241CrossRefGoogle Scholar
  33. Mitesser O., Weissel N., Strohm E. and Poethke H.J. 2006. The evolution of activity breaks in the nest cycle of annual eusocial bees: a model of delayed exponential growth. BMC Evol. Biol. 6: 1–12CrossRefGoogle Scholar
  34. Nakata K. and 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
  35. Naug D. and Wenzel J. 2006. Constraints on foraging success due to resource ecology limit colony productivity in social insects. Behav. Ecol. Sociobiol. 60: 62–68CrossRefGoogle Scholar
  36. Okuda N., Tayasu I. and Yanagisawa Y. 1998. Determinate growth in a paternal mouthbrooding fish whose reproductive success is limited by buccal capacity. Evol. Ecol. 12: 681–699CrossRefGoogle Scholar
  37. Oster G., Eshel I. and Cohen D. 1977. Worker–queen conflict and the evolution of social insects. Theor. Popul. Biol. 12: 49–85PubMedCrossRefGoogle Scholar
  38. Oster G.F. and Wilson E.O. 1978 Caste and Ecology in the Social Insects. Princeton University Press, Princeton. 352 ppGoogle Scholar
  39. Perrin N. and Sibly R.M. 1993. Dynamic-models of energy allocation and investment. Annu. Rev. Ecol. Syst. 24: 379–410CrossRefGoogle Scholar
  40. Perrin N., Sibly R.M. and Nichols N.K. 1993. Optimal-growth strategies when mortality and production-rates are size-dependent. Evol. Ecol. 7: 576–592CrossRefGoogle Scholar
  41. Queller D.C. 1989. The evolution of eusociality—reproductive head starts of workers. Proc. Natl. Acad. Sci. USA 86: 3224–3226PubMedCrossRefGoogle Scholar
  42. Reeve H.K. and Keller L. 1999 Levels of selection: burying the units of selection debate and unearthing the crucial new issues. In: Levels of Selection in Evolution (L. Keller, Ed.). Princeton University Press, Princeton. pp 3–15Google Scholar
  43. Roff D.A. 2002 Life History Evolution. Sinauer Associates, Sunderland. 527 ppGoogle Scholar
  44. Roff D.A., Heibo E. and Vollestad L.A. 2006. The importance of growth and mortality costs in the evolution of the optimal life history. J. Evol. Biol. 19: 1920–1930PubMedCrossRefGoogle Scholar
  45. Schmid-Hempel P. 1998 Parasites in Social Insects. Princeton University Press, Princeton. 392 ppGoogle Scholar
  46. Schmid-Hempel P. and Schmid-Hempel R. 1984. Life duration and turnover of foragers in the ant Cataglyphis bicolor (Hymenoptera, Formicidae). Insect. Soc. 31: 350–360CrossRefGoogle Scholar
  47. Shreeves G. and Field J. 2002. Group size and direct fitness in social queues. Am. Nat. 159: 81–95PubMedCrossRefGoogle Scholar
  48. Smith A.R., Wcislo W.T., Donnell S.O. 2007. Survival and productivity benefits to social nesting in the sweat bee Megalopta genalis (Hymenoptera: Halictidae). Behav. Ecol. Sociobiol. 61: 1111–1120CrossRefGoogle Scholar
  49. Stearns S.C. 1992 The Evolution of Life Histories. Oxford University Press, Oxford. 249 ppGoogle Scholar
  50. Stearns S.C. 2000. Life history evolution: successes, limitations, and prospects. Naturwissenschaften 87: 476–486PubMedCrossRefGoogle Scholar
  51. Stevens M., Hogendoorn K. and Schwarz M. 2007. Evolution of sociality by natural selection on variances in reproductive fitness: evidence from a social bee. BMC Evol. Biol. 7: 153PubMedCrossRefGoogle Scholar
  52. Strassmann J. 1985. Worker mortality and the evolution of castes in the social wasp Polistes exclamans. Insect. Soc. 32: 275–285CrossRefGoogle Scholar
  53. Strassmann J.E., Queller Q.C. and Hughes C.R. 1988. Predation and the evolution of sociality in the paper wasp Polistes bellicosus. Ecology 69: 1497–1505CrossRefGoogle Scholar
  54. Strohm E. and Bordon-Hauser A. 2003. Advantages and disadvantages of large colony size in a halictid bee: the queen’s perspective. Behav. Ecol. 14: 546–553CrossRefGoogle Scholar
  55. Sugiyama H. and Hirose T. 1991. Growth schedule of Xanthium canadense—does it optimize the timing of reproduction? Oecologia 88: 55–60CrossRefGoogle Scholar
  56. Thomas M.L. 2003. Seasonality and colony-size effects on the life-history characteristics of Rhytidoponera metallica in temperate south-eastern Australia. Aust. J. Zool. 51: 551–567CrossRefGoogle Scholar
  57. Tindo M., Keene M. and Dejean A. 2008. Advantages of multiple foundress colonies in Belonogaster juncea juncea l.: greater survival and increased productivity. Ecol. Entomol. 33: 293–297Google Scholar
  58. Tschinkel W.R. 1991. Insect sociometry, a field in search of data. Insect. Soc. 38: 77–82CrossRefGoogle Scholar
  59. Tschinkel W.R. 1993. Sociometry and sociogenesis of colonies of the fire ant Solenopsis invicta during one annual cycle. Ecol. Mon. 63: 425–457CrossRefGoogle Scholar
  60. Tschinkel W.R. 1999. Sociometry and sociogenesis of colony-level attributes of the Florida harvester ant (Hymenoptera: Formicidae). Ann. Entomol. Soc. Am. 92: 80–89Google Scholar
  61. Verhulst P.F. 1838. Notice sur la loi que la population poursuit dans son accroissement. Correspondance mathématique et physique 10: 113–121Google Scholar
  62. Worley A.C. and Harder L.D. 1996. Size-dependent resource allocation and costs of reproduction in Pinguicula vulgaris (Lentibulariaceae). J. Ecol. 84: 195–206CrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  1. 1.Field Station FabrikschleichachUniversity of WürzburgRauhenebrachGermany

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