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Cooperation facilitates the colonization of harsh environments

Nature Ecology & Evolution volume 1, Article number: 0057 (2017) | Download Citation

Abstract

Animals living in harsh environments, where temperatures are hot and rainfall is unpredictable, are more likely to breed in cooperative groups. As a result, harsh environmental conditions have been accepted as a key factor explaining the evolution of cooperation. However, this is based on evidence that has not investigated the order of evolutionary events, so the inferred causality could be incorrect. We resolved this problem using phylogenetic analyses of 4,707 bird species and found that causation was in the opposite direction to that previously assumed. Rather than harsh environments favouring cooperation, cooperative breeding has facilitated the colonization of harsh environments. Cooperative breeding was, in fact, more likely to evolve from ancestors occupying relatively cool environmental niches with predictable rainfall, which had low levels of polyandry and hence high within-group relatedness. We also found that polyandry increased after cooperative breeders invaded harsh environments, suggesting that when helpers have limited options to breed independently, polyandry no longer destabilizes cooperation. This provides an explanation for the puzzling cases of polyandrous cooperative breeding birds. More generally, this illustrates how cooperation can play a key role in invading ecological niches, a pattern observed across all levels of biological organization from cells to animal societies.

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References

  1. 1.

    The Insect Societies (Cambridge Univ. Press, 1971).

  2. 2.

    & Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr. Biol. 21, 72–78 (2011).

  3. 3.

    & Cooperative Breeding in Vertebrates (Cambridge Univ. Press, 2016).

  4. 4.

    & Temporal environmental variability drives the evolution of cooperative breeding in birds. Curr. Biol. 17, 1414–1419 (2007).

  5. 5.

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

  6. 6.

    & Cooperative breeding in birds: the role of ecology. Behav. Ecol. 10, 465–471 (1999).

  7. 7.

    & Towards a unified theory of cooperative breeding: the role of ecology and life history re-examined. Proc. R. Soc. Lond. B 267, 2411–2418 (2000).

  8. 8.

    & The relationship between ecology and the optimal helping strategy in cooperative breeders. J. Theor. Biol. 354, 25–34 (2014).

  9. 9.

    , & Helpers in colonial cooperatively breeding sociable weavers Philetairus socius contribute to buffer the effects of adverse breeding conditions. Behav. Ecol. Sociobiol. 63, 103–112 (2008).

  10. 10.

    Spatiotemporal environmental variation, risk aversion, and the evolution of cooperative breeding as a bet-hedging strategy. Proc. Natl Acad. Sci. USA 108, 10816–10822 (2011).

  11. 11.

    & Ecological constraints, life history traits and the evolution of cooperative breeding. Anim. Behav. 59, 1079–1086 (2000).

  12. 12.

    & Sex ratio and habitat limitation promote delayed dispersal in superb fairy-wrens. Nature 348, 541–542 (1990).

  13. 13.

    Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358, 493–495 (1992).

  14. 14.

    , & Helpers in a cooperatively breeding cichlid stay and pay or disperse and breed, depending on ecological constraints. Proc. R. Soc. Lond. B 272, 325–331 (2005).

  15. 15.

    & Disentangling the Correlated Evolution of Monogamy and Cooperation. Trends Ecol. Evol. 31, 503–513 (2016).

  16. 16.

    & Fluctuating environments, sexual selection and the evolution of flexible mate choice in birds. PLoS One 7, e32311 (2012).

  17. 17.

    , & Trading up: The fitness consequences of divorce in monogamous birds. Biol. Rev. 90, 1015–1034 (2015).

  18. 18.

    The genetical evolution of social behaviour. I & II. J. Theor. Biol. 7, 1–16 (1964).

  19. 19.

    Group Selection and Kin Selection. Nature 201, 1145–1147 (1964).

  20. 20.

    Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (Springer, 2014).

  21. 21.

    , , & Predictability, constancy, and contingency of periodic phenomena. Ecology 55, 1148–1153 (1974).

  22. 22.

    , , & Environmental harshness is positively correlated with intraspecific divergence in mammals and birds. Mol. Ecol. 23, 259–268 (2014).

  23. 23.

    , , & Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216 (2008).

  24. 24.

    & Cooperative breeding and monogamy in mammalian societies. Proc. R. Soc. Lond. B 279, 2151–2156 (2012).

  25. 25.

    , , & Promiscuity and the evolutionary transition to complex societies. Nature 466, 969–972 (2010).

  26. 26.

    Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17, 673–683 (2007).

  27. 27.

    , & Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95–108 (2004).

  28. 28.

    & The Major Transitions in Evolution (Oxford Univ. Press, 1995).

  29. 29.

    Principles of Social Evolution (Oxford Univ. Press, 2011).

  30. 30.

    & Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis. Proc. R. Soc. Lond. B 277, 575–584 (2010).

  31. 31.

    et al. Climate-mediated cooperation promotes niche expansion in burying beetles. eLife 2014, 1–15 (2014).

  32. 32.

    One Plus One Equals One: Symbiosis and the Evolution of Complex Life (Oxford Univ. Press, 2014).

  33. 33.

    Prevalence of different modes of parental care in birds. Proc. R. Soc. Lond. B 273, 1375–1383 (2006).

  34. 34.

    Evolutionary routes to non-kin cooperative breeding in birds. Proc. R. Soc. Lond. B 280, 1830–1833 (2013).

  35. 35.

    , , & Sex. long life and the evolutionary transition to cooperative breeding in birds. Proc. R. Soc. Lond. B 282, 1–7 (2015).

  36. 36.

    , & Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11, 2195–2212 (2002).

  37. 37.

    & Extrapair paternity, migration, and breeding synchrony in birds. Behav. Ecol. 15, 41–57 (2004).

  38. 38.

    , , & Updated high-resolution grids of monthly climatic observations – the CRU TS3.10 Dataset. Int. J. Climatol. 34, 623–642 (2014).

  39. 39.

    , , , & The global diversity of birds in space and time. Nature 491, 444–448 (2012).

  40. 40.

    , , & Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).

  41. 41.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2015).

  42. 42.

    MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

  43. 43.

    & Warnes and Raftery’s MCGibbsit MCMC diagnostic (2013);

  44. 44.

    , , & CODA: convergence diagnosis and output analysis for MCMC. R News 6, 7–11 (2006).

  45. 45.

    & Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–511 (1992).

  46. 46.

    , & Comparing parent-offspring regression with frequentist and Bayesian animal models to estimate heritability in wild populations: a simulation study for Gaussian and binary traits. Methods Ecol. Evol. 4, 260–275 (2013).

  47. 47.

    & Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am. Nat. 167, 808–825 (2006).

  48. 48.

    & in Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (ed. Garamszegi, L. Z. ) 231–262 (Springer, 2014).

  49. 49.

    & Disentangling evolutionary cause-effect relationships with phylogenetic confirmatory path analysis. Evolution 67, 378–387 (2013).

  50. 50.

    et al. CAPER: Comparative Analyses of Phylogenetics and Evolution in R. Methods Ecol. Evol. 3, 145–151 (2012).

  51. 51.

    Cause and Correlation in Biology: A User’s Guide to Path Analysis, Structural Equations and Causal Inference (Cambridge Univ. Press 2002).

  52. 52.

    Quantile Regression in R: a Vignette (2015);

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Acknowledgements

We thank the Swedish Research Council (VR), the Knut and Alice Wallenberg foundation, the Royal Society, the US National Science Foundation (IOS-1121435, IOS-1257530 and IOS-1439985) and the European Research Council for funding, and S.-F. Shen for comments.

Author information

Affiliations

  1. Department of Biology, Lund University, SE-223 62 Lund, Sweden

    • Charlie K. Cornwallis
  2. Department of Biology, Washington University, St Louis, Missouri 63130-4899, USA

    • Carlos A. Botero
  3. Department of Ecology, Evolution and Environmental Biology and Center for Integrative Animal Behavior, Columbia University, New York 10027, USA

    • Dustin R. Rubenstein
  4. Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK

    • Philip A. Downing
    • , Stuart A. West
    •  & Ashleigh S. Griffin

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Contributions

C.K.C., S.A., D.R.R. and A.S.G. conceived the study, C.K.C. analysed the data, C.A.B. and P.D. contributed materials, and all authors contributed substantially to writing the paper.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Charlie K. Cornwallis.

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DOI

https://doi.org/10.1038/s41559-016-0057