Article

Direct benefits and evolutionary transitions to complex societies

  • Nature Ecology & Evolution 1, Article number: 0137 (2017)
  • doi:10.1038/s41559-017-0137
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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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References

  1. 1.

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

  2. 2.

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

  3. 3.

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

  4. 4.

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

  5. 5.

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

  6. 6.

    , , & Ancestral Monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213–1216 (2014).

  7. 7.

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

  8. 8.

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

  9. 9.

    & Cooperative breeding in birds: a comparative test of the life history hypothesis. Proc. R. Soc. B 265, 739–745 (1998).

  10. 10.

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

  11. 11.

    & Climate and the distribution of cooperative breeding in mammals. R. Soc. Open Sci. 4, 160897 (2017).

  12. 12.

    Cryptic kin selection: kin structure in vertebrate populations and opportunities for kin-directed cooperation. Ethology 116, 203–216 (2010).

  13. 13.

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

  14. 14.

    & Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223 (1977).

  15. 15.

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

  16. 16.

    & Disentangling the correlated evolution of monogamy and cooperation. Trends Ecol. Evol. 31, 503–513 (2016).

  17. 17.

    & Reproductive skew and selection on female ornamentation in social species. Nature 462, 786–789 (2009).

  18. 18.

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

  19. 19.

    , , , & The effects of life-history and social selection on male and female plumage coloration. Nature 527, 367–370 (2015).

  20. 20.

    , , , & 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).

  21. 21.

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

  22. 22.

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

  23. 23.

    , & The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics. Hydrobiologia 615, 5–20 (2008).

  24. 24.

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

  25. 25.

    & Causes of female emigration in the group-living cichlid fish Neolamprologus multifasciatus. Ethology 108, 237–248 (2002).

  26. 26.

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

  27. 27.

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

  28. 28.

    & Helper response to experimentally manipulated predation risk in the cooperatively breeding cichlid Neolamprologus pulcher. PLoS ONE 5, e10784 (2010).

  29. 29.

    , , & Predation risk is an ecological constraint for helper dispersal in a cooperatively breeding cichlid. Proc. R. Soc. B 271, 2367–2374 (2004).

  30. 30.

    et al. Predation risk drives social complexity in cooperative breeders. Proc. Natl Acad. Sci. USA 113, 4104–4109 (2016).

  31. 31.

    , , , & A 20-year census of a rocky littoral fish community in Lake Tanganyika. Ecol. Freshw. Fish 19, 239–248 (2010).

  32. 32.

    & Life history and the evolution of family living in birds. Proc. R. Soc. B 274, 1349–1357 (2007).

  33. 33.

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

  34. 34.

    Feeding Ecology of Fish (Academic, 1994).

  35. 35.

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

  36. 36.

    , , , & Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid. Ecol. Lett. 8, 968–975 (2005).

  37. 37.

    ., & Sex. long life and the evolutionary transition to cooperative breeding in birds. Proc. R. Soc. B 282, 20151663 (2015).

  38. 38.

    , , , & Relatedness and helping in fish: examining the theoretical predictions. Proc. R. Soc. B 272, 1593–1599 (2005).

  39. 39.

    , & 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).

  40. 40.

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

  41. 41.

    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).

  42. 42.

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

  43. 43.

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

  44. 44.

    , , , & 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).

  45. 45.

    , , , & 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).

  46. 46.

    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).

  47. 47.

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

  48. 48.

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

  49. 49.

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

  50. 50.

    et al. Phylogeny and phylogeography of Altolamprologus: ancient introgression and recent divergence in a rock-dwelling Lake Tanganyika cichlid genus. Hydrobiologia 791, 35 (2016).

  51. 51.

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

  52. 52.

    & Mesquite: a modular system for evolutionary analysis v. 3.04 (2011).

  53. 53.

    , , & jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772–772 (2012).

  54. 54.

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

  55. 55.

    , , & Tracer v. 1.6 (2014).

  56. 56.

    & BayesTraits (2014).

  57. 57.

    , & APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

  58. 58.

    R Core Team. R: a language and environment for statistical computing v. 3.3.0 (2015).

  59. 59.

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

  60. 60.

    , & Bayesian estimation of ancestral character states on phylogenies. Syst. Biol. 53, 673–684 (2004).

  61. 61.

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

  62. 62.

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

  63. 63.

    & Approximate Bayesian inference with the weighted likelihood bootstrap. J. R. Stat. Soc. Ser. B 56, 3–48 (1994).

  64. 64.

    , & Bayesian selection of continuous-time Markov chain evolutionary models. Mol. Biol. Evol. 18, 1001–1013 (2001).

  65. 65.

    & Bayes factors. J. Am. Stat. Assoc. 90, 773–795 (1995).

  66. 66.

    , & Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps. Proc. R. Soc. B 282, 20150342 (2015).

  67. 67.

    & 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).

  68. 68.

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

  69. 69.

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

  70. 70.

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

  71. 71.

    & in Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (ed. Garamszegi, L. ) 201–229 (Springer, 2014).

  72. 72.

    The evolution of cooperative breeding in birds: kinship, dispersal and life history. Phil. Trans. R. Soc. B 364, 3217–3227 (2009).

  73. 73.

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

  74. 74.

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

  75. 75.

    The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology 94, 560–564 (2013).

  76. 76.

    Uninformative parameters and model selection using Akaike’s information criterion. J. Wildl. Manage. 74, 1175–1178 (2010).

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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.).

Author information

Author notes

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

    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).

Affiliations

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

    • Cody J. Dey
    • , Constance M. O’Connor
    •  & Sigal Balshine
  2. Department of Biology, McMaster University, 1280 Main Street West, Hamilton, Ontario L8S 4K1, 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, SE-10691 Stockholm, 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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to John L. Fitzpatrick.

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