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Evolution of queen cuticular hydrocarbons and worker reproduction in stingless bees


Social insect queen pheromones can be interpreted as the queen’s means of sterilizing her workers, or as an honest signal of queen presence that benefits both parties. Co-mapping worker reproductive behaviour and queen cuticular hydrocarbon (CH) composition and quantity on a phylogeny of 21 stingless bee species showed that there are no associations between these traits. Furthermore, three species that have independently evolved facultative worker sterility are unexceptional in their queen CH. Combined, our analysis suggests that the action of stingless bee queen CHs are best interpreted as a signal of queen presence and not as a chemical contraceptive.

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Figure 1: Patterns of evolution of worker reproductive behaviour in the stingless bees (Meliponini).


  1. Nunes, T. M. et al. Sci. Rep. 4, 7449 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. van Oystaeyen, A. et al. Science 343, 287–290 (2014).

    Article  CAS  PubMed  Google Scholar 

  3. Peso, M., Elgar, M. A. & Barron, A. B. Biol. Rev. 90, 542–559 (2015).

    Article  PubMed  Google Scholar 

  4. Grüter, C. & Keller, L. Curr. Opin. Neurobiol. 38, 6–11 (2016).

    Article  PubMed  Google Scholar 

  5. Oi, C. A. et al. Bioessays 37, 808–821 (2015).

    Article  CAS  PubMed  Google Scholar 

  6. Strauss, K. et al. Behav. Ecol. Sociobiol. 16, 1523–1531 (2008).

    Article  Google Scholar 

  7. Keller, L. & Nonacs, P. Anim. Behav. 45, 787–794 (1993).

    Article  Google Scholar 

  8. Ronai, I., Vergoz, V. & Oldroyd, B. P. Adv. Stud. Behav. 48, 251–317 (2016).

    Article  Google Scholar 

  9. Kerr, W. E. & Maule, V. J. New York Entomol. Soc. 72, 2–18 (1964).

    Google Scholar 

  10. Palmer, K. A., Oldroyd, B. P., Quezada-Euán, J. J. V., Paxton, R. J. & May-Itza, W. D. Mol. Ecol. 11, 2107–2113 (2002).

    Article  CAS  PubMed  Google Scholar 

  11. Ratnieks, F. L. W. Am. Nat. 132, 217–236 (1988).

    Article  Google Scholar 

  12. Hammond, R. L. & Keller, L. PLoS Biol. 2, e248 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Wenseleers, T., Helanterä, H., Alves, D. A., Dueñez-Guzmán, E. & Pamilo, P. Biol. Lett. 9, 20130334 (2013).

  14. Tóth, E., Queller, D. C., Dollin, A. & Strassmann, J. E. Insect. Soc. 51, 1–11 (2004).

    Article  Google Scholar 

  15. Rasmussen, C. & Cameron, S. A. Biol. J. Linn. Soc. 99, 206–232 (2010).

    Article  Google Scholar 

  16. Harvey, P. H . & Pagel, M. D. The Comparative Method in Evolutionary Biology (Oxford Univ. Press, 1991).

    Google Scholar 

  17. Nunes, T. M., Turatti, I. C. C., Lopes, N. P. & Zucchi, R. J. Chem. Ecol. 35, 1172–1180 (2009).

    Article  CAS  PubMed  Google Scholar 

  18. Ives, A. R. & Garland, T. J. Syst. Biol. 59, 9–26 (2010).

    Article  PubMed  Google Scholar 

  19. Ho, L. S. T. & Ané, C. Syst. Biol. 63, 397–408 (2014).

    Article  PubMed  Google Scholar 

  20. Burnham, K. P . & Anderson, D. R. Model Selection and Multimodel Inference 2nd edn (Springer, 2002).

    Google Scholar 

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The authors are grateful to E.A.B. Almeida (FFCLRP - Universidade de São Paulo) for his important contributions regarding the interpreting and coding of characters, and the analysis of phylogenetic comparative data, which were crucial to the initial development of this study. The authors are also thankful to T. Heard for providing Australian stingless bees queens. This research was supported by FAPESP (L.G.E. 2013/ 01918-1; T.M.N. 2013/09263-4, N.P.L. 2014/50265-3) and CNPq (T.M.N. 165823/2015-1).

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Authors and Affiliations



T.M.N., L.G.E. and N.P.L. designed and conceived the study. T.M.N. and S.M. collected the biological material and performed behavioural analysis on worker oviposition. T.M.N., I.C.T. and N.P.L. performed gas chromatography mass spectrometry analyses. T.M.N. and L.G.E. performed phylogenetic and statistical analyses. B.P.O. determined the conceptual framework for the paper, and T.M.N., L.G.E. and B.P.O. wrote the paper.

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Correspondence to Túlio M. Nunes.

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The authors declare no competing financial interests.

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Supplementary Methods, Supplementary Tables 1–5, two Supplementary Figures and Supplementary References. (PDF 623 kb)

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Nunes, T., Oldroyd, B., Elias, L. et al. Evolution of queen cuticular hydrocarbons and worker reproduction in stingless bees. Nat Ecol Evol 1, 0185 (2017).

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