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Direct benefits and evolutionary transitions to complex societies

Nature Ecology & Evolution volume 1, Article number: 0137 (2017) Cite this article

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An Author Correction to this article was published on 13 February 2019

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Abstract

The selective forces that drive the evolution of cooperation have been intensely debated. Evolutionary transitions to cooperative breeding, a complex form of cooperation, have been hypothesized to be linked to low degrees of promiscuity, which increases intragroup relatedness and the indirect (that is, kin selected) benefits of helping. However, ecological factors also promote cooperative breeding, and may be more important than relatedness in some contexts. Identifying the key evolutionary drivers of cooperative breeding therefore requires an integrated assessment of these hypotheses. Here we show, using a phylogenetic framework that explicitly evaluates mating behaviours and ecological factors, that evolutionary transitions to cooperative breeding in cichlid fishes were not associated with social monogamy. Instead, group living, biparental care and diet type directly favoured the evolution of cooperative breeding. Our results suggest that cichlid fishes exhibit an alternative path to the evolution of complex societies compared to other previously studied vertebrates, and these transitions are driven primarily by direct fitness benefits.

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Figure 1: Behavioural diversity in lamprologine cichlids.
Figure 2: Evolutionary drivers of cooperative breeding in lamprologine cichlids.
Figure 3: Contrasting sexual size dimorphism between social and mating systems in lamprologine cichlids.

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  • 13 February 2019

    In the version of this Article originally published, references were missing from the column “Source(s) for mating and parental care system data” in Supplementary Table 1. The following references have now been added to the relevant species: Brichard 1989 has been added to Chalinochromis popelini, Chalinochromis brichardi and Julidochromis dickfeldi; Clabaut et al. 2007 to Altolamprologus calvus and Julidochromis regani; Konings 1998 to Neolamprologus hecqui; and Kuwamura 1997 to Chalinochromis popelini.

References

  1. Cornwallis, C. K., West, S. A., Davis, K. E. & Griffin, A. S. Promiscuity and the evolutionary transition to complex societies. Nature466, 969–972 (2010).

    Article  CAS  PubMed  Google Scholar 

  2. Darwin, C. On the Origin of Species (John Murray, 1859).

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

    Article  CAS  PubMed  Google Scholar 

  4. 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 

  5. Boomsma, J. J. Lifetime monogamy and the evolution of eusociality. Phil. Trans. R. Soc. B 364, 3191–3207 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Hughes, W. O. H., Oldroyd, B. P., Beekman, M. & Francis, L. W. Ancestral Monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216 (2014).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  9. Arnold, K. E. & Owens, I. P. F. Cooperative breeding in birds: a comparative test of the life history hypothesis. Proc. R. Soc. B265, 739–745 (1998).

    Article  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  11. Lukas, D. & Clutton-brock, T. Climate and the distribution of cooperative breeding in mammals. R. Soc. Open Sci. 4, 160897 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  12. Hatchwell, B. J. Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation. Ethology116, 203–216 (2010).

    Article  Google Scholar 

  13. Leimar, O. & Hammerstein, P. Cooperation for direct fitness benefits. Phil. Trans. R. Soc. B 365, 2619–2626 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Emlen, S. T. & Oring, L. W. Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223 (1977).

    Article  CAS  PubMed  Google Scholar 

  15. Nonacs, P. Monogamy and high relatedness do not preferentially favor the evolution of cooperation. BMC Evol. Biol.11, 58 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Dillard, J. R. & Westneat, D. F. Disentangling the correlated evolution of monogamy and cooperation. Trends Ecol. Evol.31, 503–513 (2016).

    Article  PubMed  Google Scholar 

  17. Rubenstein, D. R. & Lovette, I. J. Reproductive skew and selection on female ornamentation in social species. Nature462, 786–789 (2009).

    Article  CAS  PubMed  Google Scholar 

  18. Young, A. J. & Bennett, N. C. Intra-sexual selection in cooperative mammals and birds: why are females not bigger and better armed? Phil. Trans. R. Soc. B 368, 20130075 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Dale, J., Dey, C., Delhey, K., Kempenaers, B. & Valcu, M. The effects of life-history and social selection on male and female plumage coloration. Nature527, 367–370 (2015).

    Article  CAS  PubMed  Google Scholar 

  20. Sturmbauer, C., Salzburger, W., Duftner, N., Schelly, R. & Koblmüller, S. Evolutionary history of the Lake Tanganyika cichlid tribe Lamprologini (Teleostei: Perciformes) derived from mitochondrial and nuclear DNA data. Mol. Phylogenet. Evol.57, 266–284 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wong, M. & Balshine, S. The evolution of cooperative breeding in the African cichlid fish, Neolamprologus pulcher. Biol. Rev. 86, 511–530 (2011).

    Article  PubMed  Google Scholar 

  22. Konings, A. Tanganyika Cichlids in Their Natural Habitat. (Cichlid, 1998).

    Google Scholar 

  23. Koblmüller, S., Sefc, K. M. & Sturmbauer, C. The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics. Hydrobiologia615, 5–20 (2008).

    Article  CAS  Google Scholar 

  24. Sefc, K. M. Mating and parental care in Lake Tanganyika’s cichlids. Int. J. Evol. Biol. 2011, 470875 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Schradin, C. & Lamprecht, J. Causes of female emigration in the group-living cichlid fish Neolamprologus multifasciatus. Ethology108, 237–248 (2002).

    Article  Google Scholar 

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

    Google Scholar 

  27. Taborsky, B. & Foerster, K. Female mouthbrooders adjust incubation duration to perceived risk of predation. Anim. Behav.68, 1275–1281 (2004).

    Article  Google Scholar 

  28. Heg, D. & Taborsky, M. Helper response to experimentally manipulated predation risk in the cooperatively breeding cichlid Neolamprologus pulcher. PLoS ONE5, e10784 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Heg, D., Bachar, Z., Brouwer, L. & Taborsky, M. Predation risk is an ecological constraint for helper dispersal in a cooperatively breeding cichlid. Proc. R. Soc. B 271, 2367–2374 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Groenewoud, F. et al. Predation risk drives social complexity in cooperative breeders. Proc. Natl Acad. Sci. USA113, 4104–4109 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Takeuchi, Y., Ochi, H., Kohda, M., Sinyinza, D. & Hori, M. A 20-year census of a rocky littoral fish community in Lake Tanganyika. Ecol. Freshw. Fish19, 239–248 (2010).

    Article  Google Scholar 

  32. Covas, R. & Griesser, M. Life history and the evolution of family living in birds. Proc. R. Soc. B274, 1349–1357 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Alexander, R. The evolution of social behavior. Annu. Rev. Ecol. Syst.5, 325–383 (1974).

    Article  Google Scholar 

  34. Gerking, S. Feeding Ecology of Fish (Academic, 1994).

    Google Scholar 

  35. Stiver, K. A. et al. Evidence for size and sex-specific dispersal in a cooperatively breeding cichlid fish. Mol. Ecol. 16, 2974–2984 (2007).

    Article  CAS  PubMed  Google Scholar 

  36. Dierkes, P., Heg, D., Taborsky, M., Skubic, E. & Achmann, R. Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid. Ecol. Lett.8, 968–975 (2005).

    Article  PubMed  Google Scholar 

  37. Downing, P. A ., Cornwallis, C. K. & Griffin, A. S. Sex. long life and the evolutionary transition to cooperative breeding in birds. Proc. R. Soc. B282, 20151663 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Stiver, K. A., Dierkes, P., Taborsky, M., Gibbs, H. L. & Balshine, S. Relatedness and helping in fish: examining the theoretical predictions. Proc. R. Soc. B272, 1593–1599 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Awata, S., Munehara, H. & Kohda, M. Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses. Behav. Ecol. Sociobiol.58, 506–516 (2005).

    Article  Google Scholar 

  40. Hellman, J. K . et al. Reproductive sharing in relation to group and colony-level attributes in a cooperative breeding fish. Proc. R. Soc. B 282, 20150954 (2015).

    Article  Google Scholar 

  41. Hellmann, J. K. et al. Within-group relatedness is correlated with colony-level social structure and reproductive sharing in a social fish. Mol. Ecol.25, 4001–4013 (2016).

    Article  CAS  PubMed  Google Scholar 

  42. Kohler, U. Zur Struktur und Evolution des Sozialsystems von Neolamprologus multifasciatus (Cichlidae, Pisces), dem kleinsten Schneckenbuntbarsch des Tanganjikasees PhD thesis, Ludwig-Maximilians Univ. (1997).

    Google Scholar 

  43. Tanaka, H. et al. Group composition, relatedness, and dispersal in the cooperatively breeding cichlid Neolamprologus obscurus. Behav. Ecol. Sociobiol.69, 169–181 (2015).

    Article  Google Scholar 

  44. Salzburger, W., Meyer, A., Baric, S., Verheyen, E. & Sturmbauer, C. Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the central and east African haplochromine cichlid fish faunas. Syst. Biol.51, 113–135 (2008).

    Article  Google Scholar 

  45. Schelly, R., Salzburger, W., Koblmüller, S., Duftner, N. & Sturmbauer, C. Phylogenetic relationships of the lamprologine cichlid genus Lepidiolamprologus (Teleostei: Perciformes) based on mitochondrial and nuclear sequences, suggesting introgressive hybridization. Mol. Phylogenet. Evol.38, 426–438 (2006).

    Article  CAS  PubMed  Google Scholar 

  46. Duftner, N. et al. Parallel evolution of facial stripe patterns in the Neolamprologus brichardi/pulcher species complex endemic to Lake Tanganyika. Mol. Phylogenet. Evol.45, 706–715 (2007).

    Article  PubMed  Google Scholar 

  47. Koblmüller, S. et al. Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika—the result of repeated introgressive hybridization. BMC Evol. Biol.7, 7 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Nevado, B. et al. Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish. Mol. Ecol. 18, 4240–4255 (2009).

    Article  CAS  PubMed  Google Scholar 

  49. Gante, H. F. et al. Genomics of speciation and introgression in Princess cichlid fishes from Lake Tanganyika. Mol. Ecol.25, 6143–6161 (2016).

    Article  PubMed  Google Scholar 

  50. Koblmüller, S. et al. Phylogeny and phylogeography of Altolamprologus: ancient introgression and recent divergence in a rock-dwelling Lake Tanganyika cichlid genus. Hydrobiologia791, 35 (2016).

    Article  CAS  Google Scholar 

  51. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Madison, W. & Madison, D. Mesquite: a modular system for evolutionary analysis v. 3.04 http://mesquiteproject.wikispaces.com/ (2011).

  53. Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods9, 772–772 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. 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  PubMed  PubMed Central  Google Scholar 

  55. Rambaut, A., Suchard, M., Xie, D. & Drummond, A. Tracer v. 1.6 http://tree.bio.ed.ac.uk/software/tracer/ (2014).

  56. Meade, M. & Pagel, M. BayesTraits (2014).

  57. Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics20, 289–290 (2004).

    Article  CAS  PubMed  Google Scholar 

  58. R Core Team. R: a language and environment for statistical computing v. 3.3.0 https://cran.r-project.org/ (2015).

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

    Article  Google Scholar 

  60. Pagel, M., Meade, A. & Barker, D. Bayesian estimation of ancestral character states on phylogenies. Syst. Biol.53, 673–684 (2004).

    Article  PubMed  Google Scholar 

  61. Nunn, C. L. The Comparative Approach in Evolutionary Anthropology and Biology (Chicago Univ. Press, 2011).

    Book  Google Scholar 

  62. 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 

  63. Newton, M. A. & Raftery, A. E. Approximate Bayesian inference with the weighted likelihood bootstrap. J. R. Stat. Soc. Ser. B56, 3–48 (1994).

    Google Scholar 

  64. Suchard, M. A., Weiss, R. E. & Sinsheimer, J. S. Bayesian selection of continuous-time Markov chain evolutionary models. Mol. Biol. Evol.18, 1001–1013 (2001).

    Article  CAS  PubMed  Google Scholar 

  65. Kass, R. E. & Raftery, A. E. Bayes factors. J. Am. Stat. Assoc. 90, 773–795 (1995).

    Article  Google Scholar 

  66. Chak, S. T., Duffy, J. E. & Rubenstein, D. R. Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps. Proc. R. Soc. B 282, 20150342 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  67. Hauber, M. E. & Lacey, E. A. Bateman’s principle in cooperatively breeding vertebrates: the effects of non-breeding alloparents on variability in female and male reproductive success. Integr. Comp. Biol.45, 903–914 (2005).

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  69. Shipley, B. A new inferential test for path models based on directed acyclic graphs. Struct. Equ. Model. 7, 206–218 (2000).

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  71. Gonzalez-Voyer, A. & von Hardenberg, A. in Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (ed. Garamszegi, L. ) 201–229 (Springer, 2014).

    Book  Google Scholar 

  72. Hatchwell, B. J. The evolution of cooperative breeding in birds: kinship, dispersal and life history. Phil. Trans. R. Soc. B364, 3217–3227 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  73. 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  PubMed  Google Scholar 

  74. Riehl, C. Living with strangers: direct benefits favour non-kin cooperation in a communally nesting bird. Proc. Biol. Sci. 278, 1728–1735 (2011).

    Article  PubMed  Google Scholar 

  75. Shipley, B. The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology94, 560–564 (2013).

    Article  PubMed  Google Scholar 

  76. Arnold, T. W. Uninformative parameters and model selection using Akaike’s information criterion. J. Wildl. Manage. 74, 1175–1178 (2010).

    Article  Google Scholar 

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Acknowledgements

We thank K. A. Garvy, J. K. Hellmann, I. Y. Ligocki, S. E. Marsh-Rollo, A. R. Reddon, J. Rozek, S. St-Cyr, J. Reynolds, M. Y. L. Wong, J. K. Desjardins, K. A. Stiver and N. Milligan for assistance with field data collection, and Zambian Department of Fisheries, University of Zambia in Lusaka, Tanganyika Science Lodge, and Kasakalawe Village for logistical support. We thank O. Leimar and H. Gante for helpful discussion and comments. Research was supported by the Natural Sciences and Engineering Research Council of Canada (C.M.O., C.J.D., S.B.), University of Manchester (H.W., J.L.F.), Hamilton Community Foundation (C.M.O.), Journal of Experimental Biology (C.M.O.), Ontario Innovation Trust (S.B.), Canadian Foundation for Innovation (S.B.) and Canada Research Chairs program (S.B.).

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Author notes

  1. Cody J. Dey & Constance M. O’Connor

    Present address: † Present addresses: Great Lakes Institute for Environmental Research, University of Windsor, 401 Sunset Avenue, Windsor, Ontario, N9B 3P4, Canada (C.J.D.). Wildlife Conservation Society of Canada, 10 Cumberland Street North, Thunder Bay, Ontario P7A 4K9, Canada (C.M.O).,

Authors and Affiliations

  1. Department of Psychology, Neuroscience, and Behaviour, McMaster University, 1280 Main Street West, Hamilton, L8S 4K1, Ontario, Canada

    Cody J. Dey, Constance M. O’Connor & Sigal Balshine

  2. Department of Biology, McMaster University, 1280 Main Street West, Hamilton, L8S 4K1, Ontario, Canada

    Cody J. Dey

  3. Computational and Evolutionary Biology, Faculty of Life Sciences, University of Manchester, Oxford Road, Manchester, M13 9PL, UK

    Holly Wilkinson, Susanne Shultz & John L. Fitzpatrick

  4. Department of Zoology/Ethology, Stockholm University, Svante Arrhenius väg 18B, Stockholm, SE-10691, Sweden

    John L. Fitzpatrick

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Contributions

C.J.D., C.M.O., S.S., S.B. and J.L.F. conceived the study; C.M.O., H.W., S.B. and J.L.F. collected the data; C.J.D., C.M.O., H.W., S.S. and J.L.F. analysed the data; C.J.D., C.M.O., S.B. and J.L.F. wrote the paper with input from the other authors.

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Correspondence to John L. Fitzpatrick.

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Dey, C., O’Connor, C., Wilkinson, H. et al. Direct benefits and evolutionary transitions to complex societies. Nat Ecol Evol 1, 0137 (2017). https://doi.org/10.1038/s41559-017-0137

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