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Tug-of-war over reproduction in a social bee

Abstract

One of the main transitions in evolution is the shift from solitary organisms to societies with reproductive division of labour1,2. Understanding social evolution requires us to determine how ecological, social and genetic factors jointly influence group stability and partitioning of reproduction between group members3,4,5,6,7,8. Here we test the role of the three key factors predicted to influence social evolution by experimentally manipulating them in a social allodapine bee. We show that increased relatedness between nestmates results in more even reproduction among group members and a greater productivity per individual. By contrast, the degree of reproductive skew is not influenced by the opportunity for solitary breeding or by the potential benefits of cooperation. Relatedness also has a positive effect on group stability and overall productivity. These findings are in line with predictions of the tug-of-war models, in which the degree of reproductive division of labour is determined primarily by selfish competition between group members. The alternative view, where the degree of reproductive skew is the outcome of a social contract between potential breeders, was not supported by the data.

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Figure 1: Reproductive skew in nests of the high- and low-relatedness treatment, and in unmanipulated control nests.
Figure 2: Correlation between relatedness and reproductive skew across all nests.
Figure 3: Reproductive skew in treatments with high or low nesting substrate availability.
Figure 4: Reproductive skew in treatments with rich and poor floral resources (high and low k, respectively).

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References

  1. Maynard Smith, J. & Szathmáry, E. The Major Transitions in Evolution (W. H. Freeman, Oxford, 1995)

    Google Scholar 

  2. Keller, L. (ed.) Levels of Selection in Evolution (Princeton Univ. Press, Princeton, 1999)

  3. Keller, L. & Reeve, H. K. Partitioning of reproduction in animal societies. Trends Ecol. Evol. 9, 98–102 (1994)

    Article  CAS  Google Scholar 

  4. Field, J., Solis, C. R., Queller, D. C. & Strassmann, J. E. Social and genetic structure of paper wasp cofoundress associations: tests of reproductive skew models. Am. Nat. 151, 545–563 (1998)

    Article  CAS  Google Scholar 

  5. Johnstone, R. A. Models of reproductive skew: a review and synthesis. Ethology 106, 5–26 (2000)

    Article  Google Scholar 

  6. Reeve, H. K. & Keller, L. Tests of reproductive-skew models in social insects. Annu. Rev. Entomol. 46, 347–385 (2001)

    Article  CAS  Google Scholar 

  7. Clutton-Brock, T. H. et al. Cooperation, control, and concession in meerkat groups. Science 291, 478–481 (2001)

    Article  ADS  CAS  Google Scholar 

  8. Haydock, J. & Koenig, W. D. Reproductive skew in the polygynandrous acorn woodpecker. Proc. Natl Acad. Sci. USA 99, 7178–7183 (2002)

    Article  ADS  CAS  Google Scholar 

  9. Vehrencamp, S. L. A model for the evolution of despotic versus egalitarian societies. Anim. Behav. 31, 667–682 (1983)

    Article  Google Scholar 

  10. Emlen, S. T. The evolution of helping. I. An ecological constraints model. Am. Nat. 119, 29–39 (1982)

    Article  Google Scholar 

  11. Reeve, H. K. & Ratnieks, F. L. W. in Queen Number and Sociality in Insects (ed. Keller, L.) 45–85 (Oxford Univ. Press, Oxford, 1993)

    Google Scholar 

  12. Johnstone, R. A. & Cant, M. A. Reproductive skew and the threat of eviction: a new perspective. Proc. R. Soc. Lond. B 266, 275–279 (1999)

    Article  Google Scholar 

  13. Reeve, H. K., Emlen, S. T. & Keller, L. Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? Behav. Ecol. 9, 267–278 (1998)

    Article  Google Scholar 

  14. Schwarz, M. P., Bull, N. J. & Hogendoorn, K. Evolution of sociality in the allodapine bees: a review of sex allocation, ecology and evolution. Insectes Soc. 45, 349–368 (1998)

    Article  Google Scholar 

  15. Silberbauer, L. X. & Schwarz, M. P. Life-cycle and social-behavior in a heathland population of the allodapine bee, Exoneura bicolor (Hymenoptera, Apidae). Insectes Soc. 42, 201–218 (1995)

    Article  Google Scholar 

  16. Schwarz, M. P. Female-biased sex-ratios in a facultatively social bee and their implications for social evolution. Evolution 48, 1684–1697 (1994)

    Article  Google Scholar 

  17. Silberbauer, L. X. Founding patterns of Exoneura bicolor in Cobboboonee State Forest, S.W. Victoria. Aust. Zool. 28, 67–73 (1992)

    Article  Google Scholar 

  18. Bull, N. J. & Schwarz, M. P. The habitat saturation hypothesis and sociality in an allodapine bee: cooperative nesting is not ‘making the best of a bad situation’. Behav. Ecol. Sociobiol. 39, 267–274 (1996)

    Article  Google Scholar 

  19. Stevens, M. I. Egg Stock Piling Strategies and Benefits to Group Living in Exoneura bicolor Smith (Apidae, Xylocopinae) Thesis, Flinders Univ. South Australia, Adelaide (1997)

    Google Scholar 

  20. Gadagkar, R., Chandrashekara, K., Chandran, S. & Bhagavan, S. Queen success is correlated with worker–brood genetic relatedness in a primitively eusocial wasp (Ropalidia marginata). Experientia 49, 714–717 (1993)

    Article  Google Scholar 

  21. Hogendoorn, K. & Zammit, J. Benefits of cooperative breeding through increased colony survival in an allodapine bee. Insectes Soc. 48, 392–397 (2001)

    Article  Google Scholar 

  22. Reeve, H. K. in The Social Biology of Wasps (eds Ross, K. G. & Matthews, R. W.) 99–148 (Cornell Univ. Press, Ithaca, 1991)

    Google Scholar 

  23. Kokko, H. Are reproductive skew models evolutionarily stable? Proc. R. Soc. Lond. B 270, 265–270 (2003)

    Article  Google Scholar 

  24. Clutton-Brock, T. H. Reproductive skew, concessions and limited control. Trends Ecol. Evol. 13, 288–292 (1998)

    Article  CAS  Google Scholar 

  25. Reeve, H. K. & Keller, L. Partitioning of reproduction in mother–daughter versus sibling associations—a test of optimal skew theory. Am. Nat. 145, 119–132 (1995)

    Article  Google Scholar 

  26. Langer, P., Molbo, D. & Keller, L. Polymorphic microsatellite loci in Allodapine bees for investigating the evolution of social behaviour. Mol. Ecol. Notes (in the press)

  27. Schwarz, M. P. Persistent multi-female nests in an Australian Allodapine bee, Exoneura bicolor (Hymenoptera, Anthophoridae). Insectes Soc. 33, 258–277 (1986)

    Article  Google Scholar 

  28. Queller, D. C. & Goodnight, K. F. Estimating relatedness using genetic markers. Evolution 43, 258–275 (1989)

    Article  Google Scholar 

  29. Nonacs, P. Measuring and using skew in the study of social behavior and evolution. Am. Nat. 156, 577–589 (2000)

    Article  Google Scholar 

  30. Fournier, D. & Keller, L. Partitioning of reproduction among queens in the Argentine ant, Linepithema humile. Anim. Behav. 62, 1039–1045 (2001)

    Article  Google Scholar 

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Acknowledgements

We thank C. Roger, P. Jordan and G. Deppierraz for help in genotyping, N. DiMarco for extractions, M. P. Schwarz for methodological advice, A. Marazzi for statistical assistance, J. Zammit, C. van der Muren, E. Geertsema and T. Taraldsrud for help in setting up field experiments, and R. Hammond, M. Chapuisat, P. Christe, S. Helms Cahan, K. Parker, D. Queller and F. Ratnieks for comments on the manuscript.

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Correspondence to Philipp Langer or Laurent Keller.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Methods

Describes additional relatedness analyses in the experiments for solitary nesting constraints (x) and for relative goup productivity (k), as well as details for genetic analyses and reproductive skew calculations. (PDF 17 kb)

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Langer, P., Hogendoorn, K. & Keller, L. Tug-of-war over reproduction in a social bee. Nature 428, 844–847 (2004). https://doi.org/10.1038/nature02431

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