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Group formation and the evolutionary pathway to complex sociality in birds

Nature Ecology & Evolution volume 4, pages 479–486 (2020)Cite this article

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Abstract

Group-living species show a diversity of social organization, from simple mated pairs to complex communities of interdependent individuals performing specialized tasks. The advantages of living in cooperative groups are well understood, but why some species breed in small aggregations while others evolve large, complex groups with clearly divided roles is unclear. We address this problem by reconstructing the evolutionary pathways to cooperative breeding across 4,730 bird species. We show that differences in the way groups form at the origin of cooperative breeding predicts the level of group complexity that emerges. Groups that originate through the retention of offspring have a clear reproductive divide with distinct breeder and helper roles. This is associated with reproductive specialization, where breeders invest more in fecundity and less in care. In contrast, groups formed through the aggregation of unrelated adults are smaller and lack specialization. These results help explain why some species have not transitioned beyond simple groups while others have taken the pathway to increased group complexity.

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Fig. 1: The diversity of social group complexity across cooperative birds.

Patrick Kavanagh (a), Bob Brewer (b), Graham Lee (c) and Andy Reago and Chrissy McClarren (d)

Fig. 2: The evolutionary origins of group formation.
Fig. 3: Evolution of divided reproduction.
Fig. 4: Evolution of task specialization.

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Data availability

All data generated and analysed during in this study are available via the Dryad Digital Repository https://doi.org/10.5061/dryad.sn02v6x11.

Code availability

The R code detailed all analyses in this study is available via the Dryad Digital Repository https://doi.org/10.5061/dryad.sn02v6x11.

References

  1. Wilson, E. O. Sociobiology (Belknap Press, 1975).

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

  3. Koenig, W. D. & Dickinson, J. L. (eds) Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution and Behavior (Cambridge Univ. Press, 2016).

  4. Brown, J. L., Brown, E. R., Brown, S. D. & Dow, D. D. Helpers: effects of experimental removal on reproductive success. Science 215, 421–422 (1982).

    Article  CAS  PubMed  Google Scholar 

  5. Heinsohn, R. Cooperative enhancement of reproductive success in white-winged choughs. Evol. Ecol. 6, 97–114 (1992).

    Article  Google Scholar 

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

    Article  Google Scholar 

  7. Covas, R., Plessis, du, M. A. & Doutrelant, C. Helpers in colonial cooperatively breeding sociable weavers Philetairus socius contribute to buffer the effects of adverse breeding conditions. Behav. Ecol. Sociol. 63, 103–112 (2008).

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  9. Sun, S.-J. et al. Climate-mediated cooperation promotes niche expansion in burying beetles. eLife 3, e02440 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Cornwallis, C. K. et al. Cooperation facilitates the colonization of harsh environments. Nat. Ecol. Evol. 1, 0057 (2017).

    Article  Google Scholar 

  11. Branstetter, M. G. et al. Dry habitats were crucibles of domestication in the evolution of agriculture in ants. Proc. R. Soc. B 284, 20170095 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Rubenstein, D. R. & Abbot, P. (eds) Comparative Social Evolution (Cambridge Univ. Press, 2017).

  13. Lukas, D. & Clutton-Brock, T. Social complexity and kinship in animal societies. Ecol. Lett. 21, 1129–1134 (2018).

    Article  PubMed  Google Scholar 

  14. Heinsohn, R., Dunn, R., Legge, S. & Double, M. Coalitions of relatives and reproductive skew in cooperatively breeding white-winged choughs. Proc. R. Soc. B 267, 243–249 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Macedo, R. H. & Bianchi, C. A. Communal breeding in tropical Guira cuckoos Guira guira: sociality in the absence of a saturated habitat. J. Avian Biol. 28, 207–215 (1997).

    Article  Google Scholar 

  16. Lima, M. R., Macedo, R. H., Muniz, L., Pacheco, A. & Graves, J. A. Group composition, mating system, and relatedness in the communally breeding Guira cuckoo (Guira guira) in central Brazil. Auk 128, 475–486 (2011).

    Article  Google Scholar 

  17. Blackmore, C. J., Peakall, R. & Heinsohn, R. The absence of sex-biased dispersal in the cooperatively breeding grey-crowned babbler. J. Anim. Ecol. 80, 69–78 (2011).

    Article  PubMed  Google Scholar 

  18. Bowen, B. D., Koford, R. R. & Vehrencamp, S. L. Dispersal in the communally breeding groove-billed ani (Crotophaga sulcirostris). Condor 91, 52–64 (1989).

    Article  Google Scholar 

  19. West, S. A., Fisher, R. M., Gardner, A. & Kiers, E. T. Major evolutionary transitions in individuality. Proc. Natl Acad. Sci. USA 112, 10112–10119 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  21. Cooper, G. A. & West, S. A. Division of labour and the evolution of extreme specialization. Nat. Ecol. Evol. 2, 1161–1167 (2018).

    Article  PubMed  Google Scholar 

  22. 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  PubMed  Google Scholar 

  23. Fisher, R. M., Cornwallis, C. K. & West, S. A. Group formation, relatedness, and the evolution of multicellularity. Curr. Biol. 23, 1120–1125 (2013).

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  25. Brown, J. L. Helping and Communal Breeding in Birds (Princeton Univ. Press, 1987).

  26. Hartley, I. R. & Davies, N. B. Limits to cooperative polyandry in birds. Proc. R. Soc. B 257, 67–73 (1994).

    Article  Google Scholar 

  27. Stacey, P. B. & Koenig, W. D. (eds) Cooperative Breeding in Birds: Long-term Studies of Ecology and Behavior (Cambridge Univ. Press, 1990).

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

    Article  PubMed  PubMed Central  Google Scholar 

  29. 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  PubMed  Google Scholar 

  30. Riehl, C. Evolutionary routes to non-kin cooperative breeding in birds. Proc. R. Soc. B 280, 20132245 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Chak, S. T. C., Duffy, J. E., Hultgren, K. M. & Rubenstein, D. R. Evolutionary transitions towards eusociality in snapping shrimps. Nat. Ecol. Evol. 1, 0096 (2017).

    Article  Google Scholar 

  32. Boomsma, J. J. Kin selection versus sexual selection: why the ends do not meet. Curr. Biol. 17, R673–R683 (2007).

    Article  CAS  PubMed  Google Scholar 

  33. 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  PubMed  Google Scholar 

  34. Davies, N. B. Dunnock Behaviour and Social Evolution (Oxford Univ. Press, 1992)

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

    Article  PubMed  PubMed Central  Google Scholar 

  36. Koenig, W. D., Shen, S., Krakauer, A. H. & Haydock. J. in Reproductive Skew in Vertebrates: Proximate and Ultimate Causes (eds Hager, R. & Jones, C. B.) 227–264 (Cambridge Univ. Press, 2009).

  37. Riehl, C. Kinship and incest avoidance drive patterns of reproductive skew in cooperatively breeding birds. Am. Nat. 190, 774–785 (2017).

    Article  PubMed  Google Scholar 

  38. Heg, D. & van Treuren, R. Female–female cooperation in polygynous oystercatchers. Nature 391, 687–691 (1998).

    Article  CAS  Google Scholar 

  39. Quinn, J. S., Haselmayer, J., Dey, C. & Jamieson, I. G. Tolerance of female co-breeders in joint-laying pukeko: the role of egg recognition and peace incentives. Anim. Behav. 83, 1035–1041 (2012).

    Article  Google Scholar 

  40. Vehrencamp, S. L. Relative fecundity and parental effort in communally nesting anis, Crotophaga sulcirostris. Science 197, 403–405 (1977).

    Article  CAS  PubMed  Google Scholar 

  41. Stearns, S. C. The Evolution of Life Histories (Oxford Univ. Press, 1992).

  42. Keller, L. & Genoud, M. Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389, 958–960 (1997).

    Article  CAS  Google Scholar 

  43. Schneirla, T. C. A comparison of species and genera in the ant subfamily Dorylinae with respect to functional pattern. Insectes Soc. 4, 259–298 (1957).

    Article  Google Scholar 

  44. Boomsma, J. J. & Gawne, R. Superorganismality and caste differentiation as points of no return: how the major evolutionary transitions were lost in translation. Biol. Rev. 98, 28–54 (2018).

    Article  Google Scholar 

  45. Alexander, R. D., Noonan, K. M. & Crespi, B. J. in The Biology of the Naked Mole-Rat (eds Sherman, P. W. et al.) 3–44 (Princeton Univ. Press, 1991).

  46. Downing, P. A., Cornwallis, C. K. & Griffin, A. S. How to make a sterile helper. Bioessays 39, 1600136 (2016).

    Google Scholar 

  47. Cockburn, A. Evolution of helping behavior in cooperatively breeding birds. Ann. Rev. Ecol. Syst. 29, 141–177 (1998).

    Article  Google Scholar 

  48. Vehrencamp, S. L. Evolutionary routes to joint-female nesting in birds. Behav. Ecol. 11, 334–344 (2000).

    Article  Google Scholar 

  49. Rubenstein, D. R., Botero, C. A. & Lacey, E. A. Discrete but variable structure of animal societies leads to the false perception of a social continuum. R. Soc. Open Sci. 3, 160147 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Downing, P. A., Griffin, A. S. & Cornwallis, C. K. Group formation and the evolutionary pathway to complex sociality in birds. Dryad Digital Repository https://doi.org/10.5061/dryad.sn02v6x11 (2019).

  51. Castro, I., Minot, E. O., Fordham, R. A. & Birkhead, T. R. Polygynandry, face-to-face copulation and sperm competition in the Hihi Notiomystis cincta (Aves: Meliphagidae). Ibis 138, 765–771 (1996).

    Article  Google Scholar 

  52. Brekke, P., Cassey, P., Ariani, C. & Ewen, J. G. Evolution of extreme-mating behaviour: patterns of extrapair paternity in a species with forced extrapair copulation. Behav. Ecol. Sociol. 67, 963–972 (2013).

    Article  Google Scholar 

  53. Brouwer, L. & Griffith, S. C. Extra-pair paternity in birds. Mol. Ecol. 28, 4864–4882 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Hadfield, J. D. & Nakagawa, S. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J. Evol. Biol. 23, 494–508 (2010).

    Article  CAS  PubMed  Google Scholar 

  55. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2013).

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

    Article  Google Scholar 

  57. Ross, L., Gardner, A., Hardy, N. & West, S. A. Ecology, not the genetics of sex determination, determines who helps in eusocial populations. Curr. Biol. 23, 2383–2387 (2013).

    Article  CAS  PubMed  Google Scholar 

  58. 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).

    Article  PubMed  Google Scholar 

  59. Meade, A. & Pagel, M. BayesTraits V3 Manual http://www.evolution.rdg.ac.uk/BayesTraitsV3.0.1/Files/BayesTraitsV3.Manual.pdf (2016).

  60. Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

  61. Koricheva, J., Gurevitch, J. & Mengersen, K. (eds) Handbook of Meta-analysis in Ecology and Evolution (Princeton Univ. Press, 2013).

  62. Rosenthal, R. Meta-analytic Procedures for Social Research (Sage Publications, 1991).

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Acknowledgements

We thank S. West and G. Wild for providing comments on the manuscript. We also thank the Swedish research council (grant no. 2017-03880), the Knut and Alice Wallenberg Foundation (grant no. 2018.0138), a National Environment Research Council studentship and a Royal Society University Research Fellowship for funding.

Author information

Author notes

  1. These authors contributed equally: Ashleigh S. Griffin, Charlie K. Cornwallis.

Authors and Affiliations

  1. Department of Biology, Lund University, Lund, Sweden

    Philip A. Downing & Charlie K. Cornwallis

  2. Department of Zoology, University of Oxford, Oxford, UK

    Ashleigh S. Griffin

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Contributions

A.S.G., C.K.C. and P.A.D. conceived the study. P.A.D. designed the study and collected the data. P.A.D. and C.K.C. analysed the data. All authors contributed to writing the manuscript.

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Correspondence to Philip A. Downing.

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The authors declare no competing interests.

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Extended data

Extended Data Fig. 1 The evolution of group size.

Differences in the maximum (a) and mean (b) group sizes of family and non-family groups. Dots represent raw data for individual species with the back transformed mode and 95% CI estimated using a BPMM.

Extended Data Fig. 2 Patterns of survival in groups.

(a) The change in survival in relation to group size (Zr) in family and non-family groups. (b) The relationship between the change in survival in relation to group size (Zr) and how maternal care changes with group size (Zr). In larger family groups (blue dots) survival increases and maternal care decreases. Dots represent raw data for individual species and parameter estimates are the back transformed posterior mode and 95% CI estimated using BPMMs.

Extended Data Fig. 3

Publication bias tests and heterogeneity for each of the Fisher Z transformed correlation coefficients used as effect sizes in our study.

Supplementary information

Supplementary Information

Supplementary methods and Tables 6–8.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–5, 9 and 10.

Supplementary Data 1

Details of how each effect size used in the analyses was calculated.

Supplementary Data 2

R code needed to recreate the analyses.

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Downing, P.A., Griffin, A.S. & Cornwallis, C.K. Group formation and the evolutionary pathway to complex sociality in birds. Nat Ecol Evol 4, 479–486 (2020). https://doi.org/10.1038/s41559-020-1113-x

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