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Big brains stabilize populations and facilitate colonization of variable habitats in birds

Abstract

The cognitive buffer hypothesis posits that environmental variability can be a major driver of the evolution of cognition because an enhanced ability to produce flexible behavioural responses facilitates coping with the unexpected. Although comparative evidence supports different aspects of this hypothesis, a direct connection between cognition and the ability to survive a variable and unpredictable environment has yet to be demonstrated. Here, we use complementary demographic and evolutionary analyses to show that among birds, the mechanistic premise of this hypothesis is well supported but the implied direction of causality is not. Specifically, we show that although population dynamics are more stable and less affected by environmental variation in birds with larger relative brain sizes, the evolution of larger brains often pre-dated and facilitated the colonization of variable habitats rather than the other way around. Our findings highlight the importance of investigating the timeline of evolutionary events when interpreting patterns of phylogenetic correlation.

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Fig. 1: Graphical representation of our method for estimating and comparing population dynamics of North American birds.
Fig. 2: Significant two-way interactions between species traits and environmental variability on population stability.
Fig. 3: Testing the sequence of evolutionary events predicted by the cognitive buffer and colonization advantage hypotheses.
Fig. 4: Ancestral trait reconstruction of relative brain size and environmental niche.

References

  1. 1.

    Bennett, P. M. & Harvey, P. H. Relative brain size and ecology in birds. J. Zool. 207, 151–169 (1985).

    Google Scholar 

  2. 2.

    Isler, K. & van Schaik, C. P. Metabolic costs of brain size evolution. Biol. Lett. 2, 557–560 (2006).

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Iwaniuk, A. N. & Nelson, J. E. Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can. J. Zool. 81, 1913–1928 (2003).

    Google Scholar 

  4. 4.

    Barton, R. A. & Capellini, I. Maternal investment, life histories, and the costs of brain growth in mammals. Proc. Natl Acad. Sci. USA 108, 6169–6174 (2011).

    CAS  PubMed  Google Scholar 

  5. 5.

    Sol, D. in Cognitive Ecology II (eds Dukas, R. & Ratcliffe, J. M.) 111–134 (Univ. Chicago Press, Chicago, 2009).

  6. 6.

    Potts, R. Variability selection in hominid evolution. Evol. Anthropol. 7, 81–96 (1998).

    Google Scholar 

  7. 7.

    Reader, S. M. & Laland, K. N. Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl Acad. Sci. USA 99, 4436–4441 (2002).

    CAS  PubMed  Google Scholar 

  8. 8.

    Lefebvre, L. Brains, innovations, tools and cultural transmission in birds, non-human primates, and fossil hominins. Front. Hum. Neurosci. 7, 245 (2013).

    PubMed  PubMed Central  Google Scholar 

  9. 9.

    Sol, D., Székely, T., Liker, A. & Lefebvre, L. Big-brained birds survive better in nature. Proc. R. Soc. B 274, 763–769 (2007).

    PubMed  Google Scholar 

  10. 10.

    Maille, A. & Schradin, C. Survival is linked with reaction time and spatial memory in African striped mice. Biol. Lett. 12, 20160346 (2016).

    PubMed  PubMed Central  Google Scholar 

  11. 11.

    Shultz, S., Bradbury, R. B., Evans, K. L., Gregory, R. D. & Blackburn, T. M. Brain size and resource specialization predict long-term population trends in British birds. Proc. R. Soc. B 272, 2305–2311 (2005).

    PubMed  Google Scholar 

  12. 12.

    Maklakov, A. A., Immler, S., Gonzalez-Voyer, A., Rönn, J. & Kolm, N. Brains and the city: big-brained passerine birds succeed in urban environments. Biol. Lett. 7, 730–732 (2011).

    PubMed  PubMed Central  Google Scholar 

  13. 13.

    Vincze, O. Light enough to travel or wise enough to stay? Brain size evolution and migratory behavior in birds. Evolution 70, 2123–2133 (2016).

    PubMed  Google Scholar 

  14. 14.

    Sayol, F. et al. Environmental variation and the evolution of large brains in birds. Nat. Commun. 7, 13971 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Sol, D., Bacher, S., Reader, S. M., Lefebvre, L. & Price, S. E. T. D. Brain size predicts the success of mammal species introduced into novel environments. Am. Nat. 172, S63–S71 (2008).

    PubMed  Google Scholar 

  16. 16.

    Sol, D. et al. Unraveling the life history of successful invaders. Science 337, 580–583 (2012).

    CAS  PubMed  Google Scholar 

  17. 17.

    Amiel, J. J., Tingley, R. & Shine, R. Smart moves: effects of relative brain size on establishment success of invasive amphibians and reptiles. PLoS ONE 6, e18277 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Lefebvre, L. & Sol, D. Brains, lifestyles and cognition: are there general trends? Brain Behav. Evol. 72, 135–144 (2008).

    PubMed  Google Scholar 

  19. 19.

    Kotrschal, A., Corral-Lopez, A., Amcoff, M. & Kolm, N. A larger brain confers a benefit in a spatial mate search learning task in male guppies. Behav. Ecol. 26, 527–532 (2015).

    PubMed  Google Scholar 

  20. 20.

    Kotrschal, A. et al. Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr. Biol. 23, 168–171 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Lefebvre, L., Reader, S. M. & Sol, D. Brains, innovations and evolution in birds and primates. Brain Behav. Evol. 63, 233–246 (2004).

    PubMed  Google Scholar 

  22. 22.

    Sol, D., Lefebvre, L. & Rodríguez-Teijeiro, J. D. Brain size, innovative propensity and migratory behaviour in temperate Palaearctic birds. Proc. R. Soc. B 272, 1433–1441 (2005).

    PubMed  Google Scholar 

  23. 23.

    Sauer, J. R., Fallon, J. E. & Johnson, R. Use of North American Breeding Bird Survey data to estimate population change for bird conservation regions. J. Wildlife Manage. 67, 372–389 (2003).

    Google Scholar 

  24. 24.

    Sauer, J. R. et al. The North American Breeding Bird Survey: Results and Analysis 1966–2015 Version 2.07.2017 (USGS Patuxent Wildlife Research Center, 2017); http://www.mbr-pwrc.usgs.gov/bbs/.

    Google Scholar 

  25. 25.

    Smith, A. C., Hudson, M.-A. R., Downes, C. & Francis, C. M. Estimating breeding bird survey trends and annual indices for Canada: how do the new hierarchical Bayesian estimates differ from previous estimates? Can. Field Nat. 128, 119–134 (2014).

    Google Scholar 

  26. 26.

    Clark, J. R. et al. North American Bird Conservation Initiative: Bird Conservation Region Descriptions, a Supplement to the North American Bird Conservation Initiative Bird Conservation Regions Map (US NABCI Committee, Washington DC, 2000).

  27. 27.

    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).

    CAS  PubMed  Google Scholar 

  28. 28.

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

    Google Scholar 

  29. 29.

    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).

    PubMed  Google Scholar 

  30. 30.

    Sheehan, M. J. et al. Different axes of environmental variation explain the presence vs. extent of cooperative nest founding associations in Polistes paper wasps. Ecol. Lett. 18, 1057–1067 (2015).

    PubMed  PubMed Central  Google Scholar 

  31. 31.

    Bjørnstad, O. N. & Grenfell, B. T. Noisy clockwork: time series analysis of population fluctuations in animals. Science 293, 638–643 (2001).

    PubMed  Google Scholar 

  32. 32.

    Ricklefs, R. E. & Scheuerlein, A. Comparison of aging-related mortality among birds and mammals. Exp. Gerontol. 36, 845–857 (2001).

    CAS  PubMed  Google Scholar 

  33. 33.

    McNab, B. K. Food habits, energetics, and the population biology of mammals. Am. Nat. 116, 106–124 (1980).

    Google Scholar 

  34. 34.

    Lindstedt, S. L. & Boyce, M. S. Seasonality, fasting endurance, and body size in mammals. Am. Nat. 125, 873–878 (1985).

    Google Scholar 

  35. 35.

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

    CAS  PubMed  Google Scholar 

  36. 36.

    Devictor, V., Julliard, R. & Jiguet, F. Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117, 507–514 (2008).

    Google Scholar 

  37. 37.

    Ives, A., Dennis, B., Cottingham, K. & Carpenter, S. Estimating community stability and ecological interactions from time-series data. Ecol. Monogr. 73, 301–330 (2003).

    Google Scholar 

  38. 38.

    Dennis, B., Ponciano, J. M., Lele, S. R., Taper, M. L. & Staples, D. F. Estimating density dependence, process noise, and observation error. Ecol. Monogr. 76, 323–341 (2006).

    Google Scholar 

  39. 39.

    Sauer, J. R. & Link, W. A. Analysis of the North American Breeding Bird Survey using hierarchical models. Auk 128, 87–98 (2011).

    Google Scholar 

  40. 40.

    Brook, B. W. & Bradshaw, C. J. A. Strength of evidence for density dependence in abundance time series of 1198 species. Ecology 87, 1445–1451 (2006).

    PubMed  Google Scholar 

  41. 41.

    Ishida, Y. et al. Genetic connectivity across marginal habitats: the elephants of the Namib Desert. Ecol. Evol. 6, 6189–6201 (2016).

    PubMed  PubMed Central  Google Scholar 

  42. 42.

    Pagel, M. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. B 255, 37–45 (1994).

    Google Scholar 

  43. 43.

    Green, D. M. The ecology of extinction: population fluctuation and decline in amphibians. Biol. Conserv. 111, 331–343 (2003).

    Google Scholar 

  44. 44.

    Wells, J. C. K. & Stock, J. T. The biology of the colonizing ape. Am. J. Phys. Anthropol. 134, 191–222 (2007).

    Google Scholar 

  45. 45.

    Roth, T. C., LaDage, L. D., Freas, C. A. & Pravosudov, V. V. Variation in memory and the hippocampus across populations from different climates: a common garden approach. Proc. R. Soc. B 279, 402–410 (2012).

    PubMed  Google Scholar 

  46. 46.

    Kozlovsky, D. Y., Branch, C. L. & Pravosudov, V. V. Problem-solving ability and response to novelty in mountain chickadees (Poecile gambeli) from different elevations. Behav. Ecol. Sociobiol. 69, 635–643 (2015).

    Google Scholar 

  47. 47.

    Benson-Amram, S., Dantzer, B., Stricker, G., Swanson, E. M. & Holekamp, K. E. Brain size predicts problem-solving ability in mammalian carnivores. Proc. Natl Acad. Sci. USA 113, 2532–2537 (2016).

    CAS  PubMed  Google Scholar 

  48. 48.

    Dunbar, R. I. M. & Shultz, S. Evolution in the social brain. Science 317, 1344–1347 (2007).

    CAS  PubMed  Google Scholar 

  49. 49.

    Emery, N. J., Seed, A. M., von Bayern, A. M. P. & Clayton, N. S. Cognitive adaptations of social bonding in birds. Phil. Trans. R. Soc. B 362, 489–505 (2007).

    PubMed  Google Scholar 

  50. 50.

    Garamszegi, L. Z., Møller, A. P. & Erritzøe, J. Coevolving avian eye size and brain size in relation to prey capture and nocturnality. Proc. R. Soc. B 269, 961–967 (2002).

    PubMed  Google Scholar 

  51. 51.

    Myhrvold, N. P. et al. An amniote life-history database to perform comparative analyses with birds, mammals, and reptiles. Ecology 96, 3109–3109 (2015).

    Google Scholar 

  52. 52.

    Iwaniuk, A. N. & Nelson, J. E. Can endocranial volume be used as an estimate of brain size in birds? Can. J. Zool. 80, 16–23 (2002).

    Google Scholar 

  53. 53.

    Sol, D. et al. Evolutionary divergence in brain size between migratory and resident birds. PLoS ONE 5, e9617 (2010).

    PubMed  PubMed Central  Google Scholar 

  54. 54.

    Lima-Ribeiro, M. S. et al. EcoClimate: a database of climate data from multiple models for past, present, and future for macroecologists and biogeographers. Biodivers. Informatics 10, 1–21 (2015).

  55. 55.

    Osborne, J. Notes on the use of data transformations. Pract. Assess. Res. Eval. 8, 1–7 (2002).

    Google Scholar 

  56. 56.

    Smith, A. C., Hudson, M.-A. R., Downes, C. M. & Francis, C. M. Change points in the population trends of aerial-insectivorous birds in North America: synchronized in time across species and regions. PLoS ONE 10, e0130768 (2015).

    PubMed  PubMed Central  Google Scholar 

  57. 57.

    Plummer, M. rjags: Bayesian Graphical Models Using MCMC (R Foundation for Statistical Computing, 2013); https://cran.r-project.org/web/packages/rjags/index.html.

    Google Scholar 

  58. 58.

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

    Google Scholar 

  59. 59.

    Gelman, A. & Rubin, D. B. Inference from iterative simulation using multiple sequences. Stat. Sci. 7, 457–472 (1992).

    Google Scholar 

  60. 60.

    Gaston, K. J. & McArdle, B. H. The temporal variability of animal abundances: measures, methods and patterns. Phil. Trans. R. Soc. B 345, 335–358 (1994).

    Google Scholar 

  61. 61.

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

    CAS  PubMed  Google Scholar 

  62. 62.

    Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E. & Challenger, W. GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131 (2008).

    CAS  PubMed  Google Scholar 

  63. 63.

    Pinheiro, J. et al. nlme: Linear and Nonlinear Mixed Effects Models. (R Foundation for Statistical Computing, Vienna, 2016); https://CRAN.R-project.org/package=nlme.

    Google Scholar 

  64. 64.

    R Development Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, Vienna, 2008).

    Google Scholar 

  65. 65.

    Orme, D. et al. The caper Package: Comparative Analysis of Phylogenetics and Evolution in R v0.5.2.. (R Foundation for Statistical Computing, Vienna, 2013. http://cran.r-project.org/web/packages/caper/index.html.

    Google Scholar 

  66. 66.

    Maddison, W. P. & FitzJohn, R. G. The unsolved challenge to phylogenetic correlation tests for categorical characters. Syst. Biol. 64, 127–136 (2015).

    PubMed  Google Scholar 

  67. 67.

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

    Google Scholar 

  68. 68.

    Pagel, M., Meade, A., Crespi, A. E. B. J. & Losos, E. J. B. Bayesian analysis of correlated evolution of discrete characters by reversible‐jump Markov chain Monte Carlo. Am. Nat. 167, 808–825 (2006).

    PubMed  Google Scholar 

  69. 69.

    Barbeitos, M. S., Romano, S. L. & Lasker, H. R. Repeated loss of coloniality and symbiosis in scleractinian corals. Proc. Natl Acad. Sci. USA 107, 11877–11882 (2010).

    CAS  PubMed  Google Scholar 

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Acknowledgements

We thank B. Carlson for invaluable feedback on an earlier draft of this manuscript. We are also grateful to the BBS and the countless volunteers that participate annually in this yearly survey. Bayesian analyses were run in the Washington University Center for High Performance Computing (CHPC), which is partially funded by NIH grants 1S10RR022984-01A1 and 1S10OD018091-01. We thank M. Tobias for his helpful advice on HPC.

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T.S.F. and C.A.B. designed analyses, compiled data and wrote the manuscript. T.S.F. additionally performed analyses and prepared figures. A.N.I. collected and compiled data, and contributed to writing.

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Correspondence to Trevor S. Fristoe.

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Supplementary Information

Supplementary Tables 1–3, Supplementary Figures 1–3

Supplementary Data 1

Data for 126 species used in population analyses. Variable descriptions can be found in the methods section of the manuscript.

Supplementary Data 2

Data for 2,062 species used in estimating relative brain sizes, including 1,288 species included in global evolutionary analyses. Variable descriptions can be found in the methods section of the manuscript.

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Fristoe, T.S., Iwaniuk, A.N. & Botero, C.A. Big brains stabilize populations and facilitate colonization of variable habitats in birds. Nat Ecol Evol 1, 1706–1715 (2017). https://doi.org/10.1038/s41559-017-0316-2

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