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Complex social behaviour derived from maternal reproductive traits


A fundamental goal of sociobiology is to explain how complex social behaviour evolves1, especially in social insects, the exemplars of social living. Although still the subject of much controversy2, recent theoretical explanations have focused on the evolutionary origins of worker behaviour (assistance from daughters that remain in the nest and help their mother to reproduce) through expression of maternal care behaviour towards siblings3,4. A key prediction of this evolutionary model is that traits involved in maternal care have been co-opted through heterochronous expression of maternal genes5 to result in sib-care, the hallmark of highly evolved social life in insects6. A coupling of maternal behaviour to reproductive status evolved in solitary insects, and was a ready substrate for the evolution of worker-containing societies3,4,7,8. Here we show that division of foraging labour among worker honey bees (Apis mellifera) is linked to the reproductive status of facultatively sterile females. We thereby identify the evolutionary origin of a widely expressed social-insect behavioural syndrome1,5,7,9, and provide a direct demonstration of how variation in maternal reproductive traits gives rise to complex social behaviour in non-reproductive helpers.

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Figure 1: Distributions of ovariole number and patterns of previtellogenic ovarian activation in worker bees.
Figure 2: Correlations between ovariole number and the social behaviour of wild-type bees.


  1. Robinson, G. E., Grozinger, C. M. & Whitfield, C. W. Sociogenomics: social life in molecular terms. Nature Rev. Genet. 6, 257–270 (2005)

    Article  CAS  Google Scholar 

  2. Wilson, E. O. & Hölldobler, B. Eusociality: origin and consequences. Proc. Natl Acad. Sci. USA 102, 13367–13371 (2005)

    Article  ADS  CAS  Google Scholar 

  3. West-Eberhard, M. J. in Animal Societies: Theories and Fact (eds Itô, Y., Brown, J. L. & Kikkawa, J.) 35–51 (Japan Sci. Soc. Press, Tokyo, 1987)

    Google Scholar 

  4. West-Eberhard, M. J. in Natural History and Evolution of Paper Wasp (eds Turillazzi, S. & West-Eberhard, M. J.) 290–317 (Oxford Univ. Press, New York, 1996)

    Google Scholar 

  5. Linksvayer, T. A. & Wade, M. J. The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: Maternal effects, sib-social effects, and heterochrony. Q. Rev. Biol. 80, 317–336 (2005)

    Article  Google Scholar 

  6. West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, New York, 2003)

    Google Scholar 

  7. Amdam, G. V., Norberg, K., Fondrk, M. K. & Page, R. E. Reproductive ground plan may mediate colony-level selection effects on individual foraging behaviour in honey bees. Proc. Natl Acad. Sci. USA 101, 11350–11355 (2004)

    Article  ADS  CAS  Google Scholar 

  8. Hunt, J. H. & Amdam, G. V. Bivoltinism as an antecedent to eusociality in the paper wasp genus Polistes. Science 308, 264–267 (2005)

    Article  ADS  CAS  Google Scholar 

  9. Page, R. E. & Erber, J. Levels of behavioural organization and the evolution of division of labour. Naturwissenschaften 89, 91–106 (2002)

    Article  ADS  CAS  Google Scholar 

  10. Seeley, T. D. The Wisdom of the Hive (Harvard Univ. Press, Cambridge, Massachusetts, 1995)

    Google Scholar 

  11. Robinson, G. E. Regulation of division of labour in insect societies. Annu. Rev. Entomol. 37, 637–665 (1992)

    Article  CAS  Google Scholar 

  12. Winston, M. L. The Biology of the Honey Bee (Harvard Univ. Press, Cambridge, Massachusetts, 1987)

    Google Scholar 

  13. Rueppell, O., Pankiw, T. & Page, R. E. Pleiotropy, epistasis and new QTL: The genetic architecture of honey bee foraging behaviour. J. Hered. 95, 481–491 (2004)

    Article  Google Scholar 

  14. Page, R. E. & Fondrk, M. K. 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, 135–144 (1995)

    Article  Google Scholar 

  15. Dunn, T. & Richards, M. H. When to bee social: interactions among environmental constraints, incentives, guarding, and relatedness in a facultatively social carpenter bee. Behav. Ecol. 14, 417–424 (2003)

    Article  Google Scholar 

  16. Simonet, G. et al. Neuroendocrinological and molecular aspects of insect reproduction. J. Neuroendocrinol. 16, 649–659 (2004)

    Article  CAS  Google Scholar 

  17. Min, K. J., Taub-Montemayor, T. E., Linse, K. D., Kent, J. W. & Rankin, M. A. Relationship of adipokinetic hormone I and II to migratory propensity in the grasshopper, Melanoplus sanguinipes. Arch. Insect Biochem. Physiol. 55, 33–42 (2004)

    Article  CAS  Google Scholar 

  18. Spieth, J., Nettleton, M., Zuckeraprison, E., Lea, K. & Blumenthal, T. Vitellogenin motifs conserved in nematodes and vertebrates. J. Mol. Evol. 32, 429–438 (1991)

    Article  ADS  CAS  Google Scholar 

  19. Capella, I. C. S. & Hartfelder, K. Juvenile hormone effect on DNA synthesis and apoptosis in caste-specific differentiation of the larval honey bee (Apis mellifera L.) ovary. J. Insect Physiol. 44, 385–391 (1998)

    Article  CAS  Google Scholar 

  20. Tatar, M. & Yin, C. M. Slow aging during insect reproductive diapause: why butterflies, grasshoppers and flies are like worms. Exp. Gerontol. 36, 723–738 (2001)

    Article  CAS  Google Scholar 

  21. Tu, M. P. & Tatar, M. Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster. Aging Cell 2, 327–333 (2003)

    Article  CAS  Google Scholar 

  22. Tanaka, E. D. & Hartfelder, K. The initial stages of oogenesis and their relation to differential fertility in the honey bee (Apis mellifera) castes. Arthropod Struct. Dev. 33, 431–442 (2004)

    Article  CAS  Google Scholar 

  23. Hodin, J. & Riddiford, L. M. Different mechanisms underlie phenotypic plasticity and interspecific variation for a reproductive character in drosophilids (Insecta: Diptera). Evolution 54, 1638–1653 (2000)

    Article  CAS  Google Scholar 

  24. Hartfelder, K., Bitondi, M. M. G., Santana, W. C. & Simões, Z. L. P. Ecdysteroid titer and reproduction in queens and workers of the honey bee and of a stingless bee: loss of ecdysteroid function at increasing levels of sociality? Insect Biochem. Mol. Biol. 32, 211–216 (2002)

    Article  CAS  Google Scholar 

  25. Maurizio, A. Pollenernahrung und Lebensvorgange bei der Honigbiene (Apis mellifera L.). Landwirtsch. Jahrb. Schweiz. 245, 115–182 (1954)

    Google Scholar 

  26. Hartfelder, K., Köstlin, K. & Hepperle, C. Ecdysteroid-dependent protein synthesis in caste-specific development of the larval honey bee ovary. Rouxs Arch. Dev. Biol. 205, 73–80 (1995)

    Article  CAS  Google Scholar 

  27. Butler, C. G. The control of ovary development in worker honeybees (Apis mellifera). Experientia 13, 256–257 (1957)

    Article  CAS  Google Scholar 

  28. Bloch, G., Wheeler, D. & Robinson, G. E. in Hormones, Brain and Behavior (eds Pfaff, D., Arnold, A. P., Etgen, A. M., Fahrbach, S. E. & Rubin, R. T. ) 195–235 (Academic, San Diego, 2002)

    Book  Google Scholar 

  29. Robinson, G. E. & Ben-Shahar, Y. Social behaviour and comparative genomics: new genes or new gene regulation? Genes Brain Behav. 1, 197–203 (2002)

    Article  CAS  Google Scholar 

  30. Gary, N. E. & Lorenzen, K. A method for collecting the honey-sac content from honeybees. J. Apic. Res. 15, 73–79 (1976)

    Article  Google Scholar 

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We thank A.L.O.T. Aase for assistance with dissections, and K. Hartfelder and P. Kukuk for comments. The project was supported by grants from the Norwegian Research Council to G.V.A, and from the National Institute on Aging and the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service to R.E.P.

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Correspondence to Gro V. Amdam or Robert E. Page Jr.

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Supplementary Tables

Supplementary Table 1 and 2. Detailed results on ovary size (number of ovary filaments) and state of ovarian activation in honey bee workers of strains selected for high- or low levels of pollen collection and storage. (DOC 142 kb)

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Amdam, G., Csondes, A., Fondrk, M. et al. Complex social behaviour derived from maternal reproductive traits. Nature 439, 76–78 (2006).

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