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Cooperation facilitates the colonization of harsh environments

Nature Ecology & Evolution volume 1, Article number: 0057 (2017) Cite this article

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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.

The idea that environmental conditions drive the evolution of cooperative breeding could, however, be incorrect. An alternative explanation is that causation is in the opposite direction, with cooperative breeding allowing individuals to colonize and breed in harsher environments. Another potential explanation is that there is no causal relationship between environmental conditions and cooperative breeding, and that their association is instead explained by a third correlated variable15. For example, environmental conditions can influence rates of divorce and female polyandry, both of which determine within group relatedness16,17. Relatedness is important because cooperation is more likely to be favoured if it is directed towards relatives that share the genes for cooperation18, termed kin selection19. In this case, cooperative breeding could occur more often in harsh environments simply because the environment determines rates of female polyandry and relatedness within families, rather than environmental conditions directly selecting for helping behaviour. These competing hypotheses have remained untested because reliably reconstructing the order of evolutionary events for more than two traits simultaneously is a major challenge and requires data on the all relevant variables for a large number of species20.

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Figure 1: Animals living in harsh environments are more likely to breed cooperatively.
Figure 2: Cooperative breeding and the association with harsh environments and low levels of polyandry.
Figure 3: Cooperation and the invasion of harsh environments.
Figure 4: The release of constraints on female polyandry in harsh environments.
Figure 5: Evolutionary transitions between cooperative breeding and environmental niches.

References

  1. Wilson, E. O. The Insect Societies (Cambridge Univ. Press, 1971).

    Google Scholar 

  2. Jetz, W. & Rubenstein, D. R. Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr. Biol. 21, 72–78 (2011).

    Article  CAS  Google Scholar 

  3. Koenig, W. D. & Dickinson, J. L. Cooperative Breeding in Vertebrates (Cambridge Univ. Press, 2016).

    Book  Google Scholar 

  4. Rubenstein, D. R. & Lovette, I. J. Temporal environmental variability drives the evolution of cooperative breeding in birds. Curr. Biol. 17, 1414–1419 (2007).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  6. Arnold, K. E. & Owens, I. P. F. Cooperative breeding in birds: the role of ecology. Behav. Ecol. 10, 465–471 (1999).

    Article  Google Scholar 

  7. Pen, I. & Weissing, F. J. 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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  9. Covas, R., Du Plessis, M. A. & Doutrelant, C. 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).

    Article  Google Scholar 

  10. Rubenstein, D. R. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. Pruett-Jones, S. G. & Lewis, M. J. Sex ratio and habitat limitation promote delayed dispersal in superb fairy-wrens. Nature 348, 541–542 (1990).

    Article  Google Scholar 

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

    Article  Google Scholar 

  14. Bergmüller, R., Heg, D. & Taborsky, M. 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).

    Article  Google Scholar 

  15. Dillard, J. R. & Westneat, D. F. Disentangling the Correlated Evolution of Monogamy and Cooperation. Trends Ecol. Evol. 31, 503–513 (2016).

    Article  Google Scholar 

  16. Botero, C. A. & Rubenstein, D. R. Fluctuating environments, sexual selection and the evolution of flexible mate choice in birds. PLoS One 7, e32311 (2012).

    Article  CAS  Google Scholar 

  17. Culina, A., Radersma, R. & Sheldon, B. C. Trading up: The fitness consequences of divorce in monogamous birds. Biol. Rev. 90, 1015–1034 (2015).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  19. Maynard-Smith, J. Group Selection and Kin Selection. Nature 201, 1145–1147 (1964).

    Article  Google Scholar 

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

    Book  Google Scholar 

  21. Colwell, R. K., Ecology, S., Summer, N. L. & Colwell, R. K. Predictability, constancy, and contingency of periodic phenomena. Ecology 55, 1148–1153 (1974).

    Article  Google Scholar 

  22. Botero, C. A., Dor, R., McCain, C. M. & Safran, R. J. Environmental harshness is positively correlated with intraspecific divergence in mammals and birds. Mol. Ecol. 23, 259–268 (2014).

    Article  Google Scholar 

  23. Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Ratnieks, F. L. W. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216 (2008).

    Article  CAS  Google Scholar 

  24. Lukas, D. & Clutton-Brock, T. Cooperative breeding and monogamy in mammalian societies. Proc. R. Soc. Lond. B 279, 2151–2156 (2012).

    Article  Google Scholar 

  25. Cornwallis, C. K., West, S. A., Davis, K. E. & Griffin, A. S. Promiscuity and the evolutionary transition to complex societies. Nature 466, 969–972 (2010).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  27. Hall-Stoodley, L., Costerton, J. W. & Stoodley, P. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95–108 (2004).

    Article  CAS  Google Scholar 

  28. Maynard-Smith, J. & Szathmary, E. The Major Transitions in Evolution (Oxford Univ. Press, 1995).

    Google Scholar 

  29. Bourke, A. F. G. Principles of Social Evolution (Oxford Univ. Press, 2011).

    Book  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  35. Downing, P. A., Cornwallis, C. K., Griffin, A. S. & Griffin, A. S. Sex. long life and the evolutionary transition to cooperative breeding in birds. Proc. R. Soc. Lond. B 282, 1–7 (2015).

    Article  Google Scholar 

  36. Griffith, S. C., Owens, I. P. F. & Thuman, K. A. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11, 2195–2212 (2002).

    Article  CAS  Google Scholar 

  37. Spottiswoode, C. & Møller, A. P. Extrapair paternity, migration, and breeding synchrony in birds. Behav. Ecol. 15, 41–57 (2004).

    Article  Google Scholar 

  38. Harris, I., Jones, P. D., Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations – the CRU TS3.10 Dataset. Int. J. Climatol. 34, 623–642 (2014).

    Article  Google Scholar 

  39. Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).

    Article  CAS  Google Scholar 

  40. Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).

    Article  CAS  Google Scholar 

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

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

    Article  Google Scholar 

  43. Warnes, G. R. & Burrows, R. Warnes and Raftery’s MCGibbsit MCMC diagnostic (2013); https://cran.r-project.org/web/packages/mcgibbsit/

  44. Plummer, M., Best, N., Cowles, K. & Vines, K. CODA: convergence diagnosis and output analysis for MCMC. R News 6, 7–11 (2006).

    Google Scholar 

  45. Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–511 (1992).

    Article  Google Scholar 

  46. de Villemereuil, P., Gimenez, O. & Doligez, B. 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).

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  48. Ives, A. R. & Garland, T. J. in Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (ed. Garamszegi, L. Z. ) 231–262 (Springer, 2014).

    Book  Google Scholar 

  49. Hardenberg, A. von & Gonzalez-Voyer, A. Disentangling evolutionary cause-effect relationships with phylogenetic confirmatory path analysis. Evolution 67, 378–387 (2013).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  52. Koenker, R. Quantile Regression in R: a Vignette (2015); https://cran.r-project.org/web/packages/quantreg/vignettes/rq.pdf

Download references

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.

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Authors and Affiliations

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

    Charlie K. Cornwallis

  2. Department of Biology, Washington University, St Louis, 63130-4899, Missouri, USA

    Carlos A. Botero

  3. Department of Ecology, Evolution and Environmental Biology and Center for Integrative Animal Behavior, Columbia University, 10027, New York, 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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  1. Charlie K. Cornwallis
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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.

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Correspondence to Charlie K. Cornwallis.

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Cornwallis, C., Botero, C., Rubenstein, D. et al. Cooperation facilitates the colonization of harsh environments. Nat Ecol Evol 1, 0057 (2017). https://doi.org/10.1038/s41559-016-0057

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