Article | Published:

Tempo and timing of ecological trait divergence in bird speciation

Nature Ecology & Evolutionvolume 2pages11201127 (2018) | Download Citation


Organismal traits may evolve either gradually or in rapid pulses, but the relative importance of these modes in the generation of species differences is unclear. Additionally, while pulsed evolution is frequently assumed to be associated with speciation events, few studies have explicitly examined how the tempo of trait divergence varies with respect to different geographical phases of speciation, starting with geographic isolation and ending, in many cases, with spatial overlap (sympatry). Here we address these issues by combining divergence time estimates, trait measurements and geographic range data for 952 avian sister species pairs worldwide to examine the tempo and timing of trait divergence in recent speciation events. We show that patterns of divergence in key ecological traits are not gradual, but instead seem to follow a pattern of relative stasis interspersed with evolutionary pulses of varying magnitude. We also find evidence that evolutionary pulses generally precede sympatry, and that greater trait disparity is associated with sympatry. These findings suggest that early pulses of trait divergence promote subsequent transitions to sympatry, rather than occurring after sympatry has been established. Incorporating models with evolutionary pulses of varying magnitude into speciation theory may explain why some species pairs achieve rapid sympatry whereas others undergo prolonged geographical exclusion.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.


  1. 1.

    Mayr, E. Systematics and the Origin of Species (Columbia Univ. Press, New York, 1942).

  2. 2.

    Mayr, E. Animal Species and Evolution (Belknap Press, Cambridge, 1963).

  3. 3.

    Mayr, E. & Diamond, J. M. The Birds of Northern Melanesia: Speciation, Ecology and Biogeography (Oxford Univ. Press, Oxford, 2001).

  4. 4.

    Price, T. Speciation in Birds (Roberts and Company, Greenwood, 2008).

  5. 5.

    Weir, J. T. & Price, T. D. Limits to speciation inferred from times to secondary sympatry and ages of hybridizing species along a latitudinal gradient. Am. Nat. 177, 462–469 (2011).

  6. 6.

    Price, T. D. et al. Niche filling slows the diversification of Himalayan songbirds. Nature 509, 222–225 (2014).

  7. 7.

    Pigot, A. L. & Tobias, J. A. Species interactions constrain geographic range expansion over evolutionary time. Ecol. Lett. 16, 330–338 (2013).

  8. 8.

    MacArthur, R. & Levins, R. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101, 377–385 (1967).

  9. 9.

    Rundell, R. J. & Price, T. D. Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends Ecol. Evol. 24, 394–399 (2009).

  10. 10.

    Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, Oxford, 2000).

  11. 11.

    Bothwell, E., Montgomerie, R., Lougheed, S. C. & Martin, P. R. Closely related species of birds differ more in body size when their ranges overlap-in warm, but not cool, climates. Evolution 69, 1701–1712 (2015).

  12. 12.

    Tobias, J. A. et al. Species coexistence and the dynamics of phenotypic evolution in adaptive radiation. Nature 506, 359–363 (2014).

  13. 13.

    Pfennig, D. W. & Pfennig, K. S. Character displacement and the origins of diversity. Am. Nat. 176, S26–S44 (2010).

  14. 14.

    Hunt, G. & Rabosky, D. L. Phenotypic evolution in fossil species: pattern and process. Annu. Rev. Earth Planet. Sci. 42, 421–441 (2014).

  15. 15.

    Pennell, M. W., Harmon, L. J. & Uyeda, J. C. Is there room for punctuated equilibrium in macroevolution? Trends Ecol. Evol. 29, 23–32 (2014).

  16. 16.

    Mayr, E. in Evolution as a Process (eds Huxley, J., Hardy, A. C. & Ford, E. B.) 157–180 (Allen and Unwin, London, 1954).

  17. 17.

    Rundle, H. D. & Nosil, P. Ecological speciation. Ecol. Lett. 8, 336–352 (2005).

  18. 18.

    Futuyma, D. J. On the role of species in anagenesis. Am. Nat. 130, 465–473 (1987).

  19. 19.

    Gingerich, P. Rates of evolution: effects of time and temporal scaling. Science 222, 159–162 (1983).

  20. 20.

    Estes, S. & Arnold, S. J. Resolving the paradox of stasis: models with stabilizing selection explain evolutionary divergence on all timescales. Am. Nat. 169, 227–244 (2007).

  21. 21.

    Boag, P. T. & Grant, P. R. Intense natural selection in a population of Darwin’s finches (Geospizinae) in the Galapagos. Science 214, 82–85 (1981).

  22. 22.

    Uyeda, J. C., Hansen, T. F., Arnold, S. J. & Pienaar, J. The million-year wait for macroevolutionary bursts. Proc. Natl Acad. Sci. USA 108, 15908–15913 (2011).

  23. 23.

    Hunt, G., Hopkins, M. J. & Lidgard, S. Simple versus complex models of trait evolution and stasis as a response to environmental change. Proc. Natl Acad. Sci. USA 112, 4885–4890 (2015).

  24. 24.

    Prothero, D. R. et al. Size and shape stasis in late Pleistocene mammals and birds from Rancho La Brea during the Last Glacial–Interglacial cycle. Quat. Sci. Rev. 56, 1–10 (2012).

  25. 25.

    Rabosky, D. L. & Adams, D. C. Rates of morphological evolution are correlated with species richness in salamanders. Evolution 66, 1807–1818 (2012).

  26. 26.

    Bokma, F. Time, species, and separating their effects on trait variance in clades. Syst. Biol. 59, 602–607 (2010).

  27. 27.

    Seddon, N. et al. Sexual selection accelerates signal evolution during speciation in birds. Proc. R. Soc. B 280, 20131065 (2013).

  28. 28.

    Cooney, C. R. et al. Mega-evolutionary dynamics of the adaptive radiation of birds. Nature 542, 344–347 (2017).

  29. 29.

    Marshall, C. R. Five palaeobiological laws needed to understand the evolution of the living biota. Nat. Ecol. Evol. 1, 0165 (2017).

  30. 30.

    Etienne, R. S., Morlon, H. & Lambert, A. Estimating the duration of speciation from phylogenies. Evolution 68, 2430–2440 (2014).

  31. 31.

    Kuchta, S. R. & Wake, D. B. Wherefore and whither the ting species? Copeia 104, 189–201 (2016).

  32. 32.

    Futuyma, D. J. in Macroevolution (eds Serrelli, E. & Gontier, N.) 29–85 (Springer, Berlin, 2015).

  33. 33.

    Weir, J. T. & Wheatcroft, D. A latitudinal gradient in rates of evolution of avian syllable diversity and song length. Proc. R. Soc. B 278, 1713–1720 (2011).

  34. 34.

    Sullivan, B. L. et al. eBird: a citizen-based bird observation network in the biological sciences. Biol. Conserv. 142, 2282–2292 (2009).

  35. 35.

    Sullivan, B. L. et al. The eBird enterprise: an integrated approach to development and application of citizen science. Biol. Conserv. 169, 31–40 (2014).

  36. 36.

    Burleigh, J. G., Kimball, R. T. & Braun, E. L. Building the avian tree of life using a large-scale, sparse supermatrix. Mol. Phylogenet. Evol. 84, 53–63 (2015).

  37. 37.

    Baiser, B., Valle, D., Zelazny, Z. & Burleigh, J. G. Non-random patterns of invasion and extinction reduce phylogenetic diversity in island bird assemblages. Ecography 41, 361–374 (2017).

  38. 38.

    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).

  39. 39.

    Hunt, G., Bell, M. A. & Travis, M. P. Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage. Evolution 62, 700–710 (2008).

  40. 40.

    Arnold, S. J. Phenotypic evolution: the ongoing synthesis (American Society of Naturalists address). Am. Nat. 183, 729–746 (2014).

  41. 41.

    Bird Species Distribution Maps of the World (BirdLife International and Natureserve, 2014);

  42. 42.

    Dawideit, B. A., Phillimore, A. B., Laube, I., Leisler, B. & Böhning‐Gaese, K. Ecomorphological predictors of natal dispersal distances in birds. J. Anim. Ecol. 78, 388–395 (2009).

  43. 43.

    Claramunt, S., Derryberry, E. P., Remsen, J. V. Jr & Brumfield, R. T. High dispersal ability inhibits speciation in a continental radiation of passerine birds. Proc. R. Soc. B 279, 1567–1574 (2012).

  44. 44.

    Stephens, P. A., Sutherland, W. J. & Freckleton, R. P. What is the Allee effect? Oikos 87, 185–190 (1999).

  45. 45.

    Case, T. J., Holt, R. D., McPeek, M. A. & Keitt, T. H. The community context of species’ borders: ecological and evolutionary perspectives. Oikos 108, 28–46 (2005).

  46. 46.

    Phillimore, A. B. et al. Sympatric speciation in birds is rare: insights from range data and simulations. Am. Nat. 171, 646–657 (2008).

  47. 47.

    Nosil, P. Ecological Speciation (Oxford Univ. Press, Oxford, 2012).

  48. 48.

    Landis, M. J., Schraiber, J. G. & Liang, M. Phylogenetic analysis using Levy processes: finding jumps in the evolution of continuous traits. Syst. Biol. 62, 193–204 (2013).

  49. 49.

    Landis, M. J. & Schraiber, J. G. Pulsed evolution shaped modern vertebrate body sizes. Proc. Natl Acad. Sci. USA 114, 13224–13229 (2017).

  50. 50.

    Harmon, L. J. et al. Early bursts of body size and shape evolution are rare in comparative data. Evolution 64, 2385–2396 (2010).

  51. 51.

    Benkman, C. W. Divergent selection drives the adaptive radiation of crossbills. Evolution 57, 1176–1181 (2003).

  52. 52.

    Lamichhaney, S. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015).

  53. 53.

    Gavrilets, S. Evolution and speciation on holey adaptive landscapes. Trends Ecol. Evol. 12, 307–312 (1997).

  54. 54.

    Friis, G., Aleixandre, P., Rodríguez-Estrella, R., Navarro-Sigüenza, A. G. & Milá, B. Rapid postglacial diversification and long-term stasis within the songbird genus Junco: phylogeographic and phylogenomic evidence. Mol. Ecol. 25, 6175–6195 (2016).

  55. 55.

    Endler, J. A. Geographic Variation, Speciation, and Clines Vol. 10 (Princeton Univ. Press, Princeton, 1977).

  56. 56.

    Futuyma, D. J. Evolutionary constraint and ecological consequences. Evolution 64, 1865–1884 (2010).

  57. 57.

    Brown, W. L. & Wilson, E. O. Character displacement. Syst. Zool. 5, 49–64 (1956).

  58. 58.

    Dayan, T. & Simberloff, D. Ecological and community‐wide character displacement: the next generation. Ecol. Lett. 8, 875–894 (2005).

  59. 59.

    Davies, T. J., Meiri, S., Barraclough, T. G. & Gittleman, J. L. Species co-existence and character divergence across carnivores. Ecol. Lett. 10, 146–152 (2007).

  60. 60.

    Drury, J. P., Grether, G. F., Garland, T. & Morlon, H. An assessment of phylogenetic tools for analyzing the interplay between interspecific interactions and phenotypic evolution. Syst. Biol. 67, 413–427 (2017).

  61. 61.

    Roughgarden, J. Competition and theory in community ecology. Am. Nat. 122, 583–601 (1983).

  62. 62.

    Hudson, E. J. & Price, T. D. Pervasive reinforcement and the role of sexual selection in biological speciation. J. Hered. 105, 821–833 (2014).

  63. 63.

    Pigot, A. L. & Tobias, J. A. Dispersal and the transition to sympatry in vertebrates. Proc. R. Soc. B 282, 20141929 (2015).

  64. 64.

    Rosenzweig, M. L. Species Diversity in Space and Time (Cambridge Univ. Press, Cambridge, 1995).

  65. 65.

    Rosenblum, E. B. et al. Goldilocks meets Santa Rosalia: an ephemeral speciation model explains patterns of diversification across time scales. J. Evol. Biol. 39, 255–261 (2012).

  66. 66.

    Dynesius, M. & Jansson, R. Persistence of within‐species lineages: a neglected control of speciation rates. Evolution 68, 923–934 (2014).

  67. 67.

    Sanderson, M. R8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301–302 (2003).

  68. 68.

    Ksepka, D. & Clarke, J. Phylogenetically vetted and stratigraphically constrained fossil calibrations within Aves. Palaeontol. Electron. 18, 1–25 (2015).

  69. 69.

    Wilson, D. S. The adequacy of body size as a niche difference. Am. Nat. 109, 769–784 (1975).

  70. 70.

    Del Hoyo, J., Elliott, A., Sargatal, J., Christie, D. A. & de Juana, E. (eds) Handbook of the Birds of the World Alive (Lynx Edicions, Barcelona, 2015)..

  71. 71.

    Dunning, J. B. Body Masses of Birds of the World (Taylor and Francis Group, Boca Raton, 2008).

  72. 72.

    Dunning, J. B. Update to Body Masses of Birds of the World (Purdue University, 2016);

  73. 73.

    Schoener, T. W. The evolution of bill size differences among sympatric congeneric species of birds. Evolution 19, 189–213 (1965).

  74. 74.

    Miles, D. B. & Ricklefs, R. E. The correlation between ecology and morphology in deciduous forest passerine birds. Ecology 65, 1629–1640 (1984).

  75. 75.

    Ho, L. & Ane, C. A linear-time algorithm for Gaussian and non-Gaussian trait evolution models. Syst. Biol. 63, 397–408 (2014).

  76. 76.

    Stoddard, M. C. et al. Avian egg shape: form, function, and evolution. Science 356, 1249–1254 (2017).

  77. 77.

    Chesser, R. T. & Zink, R. M. Modes of speciation in birds: a test of Lynch’s method. Evolution 48, 490–497 (1994).

  78. 78.

    Barraclough, T. G. & Vogler, A. P. Detecting the geographical pattern of speciation from species-level phylogenies. Am. Nat. 155, 419–434 (2000).

  79. 79.

    Bull, C. Ecology of parapatric distributions. Annu. Rev. Ecol. Syst. 22, 19–36 (1991).

  80. 80.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2012).

  81. 81.

    Calcagno, V. & de Mazancourt, C. glmulti: an R package for easy automated model selection with (generalized) linear models. J. Stat. Softw. 34, 1–29 (2010).

  82. 82.

    Yasukawa, K. Male quality and female choice of mate in the red-winged blackbird (Agelaius phoeniceus). Ecology 62, 922–929 (1981).

  83. 83.

    Grant, P. R. & Grant, B. R. Hybridization, sexual imprinting, and mate choice. Am. Nat. 149, 1–28 (1997).

  84. 84.

    Lovette, I. J. & Hochachka, W. M. Simultaneous effects of phylogenetic niche conservatism and competition on avian community structure. Ecology 87, S14–S28 (2006).

Download references


We are grateful to numerous data collectors who contributed to eBird, GenBank and the CRC bird body mass dataset (see Supplementary Information). We also thank N. Alioravainen, E. Braun, S. Jones, R. Kimball, D. Ksepka, M. Neate-Clegg, A. Pigot, A. Ragsdale and G. Zhelezov for data collection and technical assistance. This work was supported by the National Science Foundation (DEB-1208428 to J.G.B.), the Natural Environment Research Council (NE/I028068/1 to J.A.T.) and the Oxford Clarendon Fund and US–UK Fulbright Commission (to C.S.).

Author information


  1. Biology Department, University of Florida, Gainesville, FL, USA

    • Jay P. McEntee
    •  & J. Gordon Burleigh
  2. Ecology and Evolutionary Biology Department, University of Arizona, Tucson, AZ, USA

    • Jay P. McEntee
  3. Department of Life Sciences, Imperial College London, Ascot, UK

    • Joseph A. Tobias
  4. School of Biology, University of St Andrews, St Andrews, Fife, UK

    • Catherine Sheard


  1. Search for Jay P. McEntee in:

  2. Search for Joseph A. Tobias in:

  3. Search for Catherine Sheard in:

  4. Search for J. Gordon Burleigh in:


J.G.B. and J.P.M. conceived the study; J.G.B., J.P.M. and J.A.T. designed the conceptual framework and analyses; J.G.B. performed dating analyses and assembled phylogenetic, occurrence and body mass information; J.A.T. and C.S. provided morphometric data; J.P.M. integrated datasets, and designed and performed statistical analyses with significant input from J.G.B., J.A.T. and C.S.; J.P.M. and C.S. produced figures and tables; J.P.M. wrote the manuscript, with significant input from all authors.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Jay P. McEntee.

Supplementary information

  1. Supplementary Information

    Supplementary Methods, Supplementary Figures, Supplementary Tables and Supplementary Code

  2. Reporting Summary

  3. Supplementary Data 1-8

    Supplementary Data 1: Sister pair dataset used for analysis of the probability of contact, and of breeding contact, by divergence time. Supplementary Data 2: Sister pair dataset used for GLM designed to find predictors associated with contact and breeding contact. Supplementary Data 3: Sister pairs in contact, used for GLM designed to find predictors associated with sympatry given contact. Supplementary Data 4: Morphological measurements by species. Supplementary Data 5: Log body mass divergence by species pair, used for analyses of body mass divergence tempo and mode. Supplementary Data 6: Species pairs from Burleigh et al. 2015 phylogeny excluded from co-occurrence analyses, with reasons for exlcusion. Supplementary Data 7: Fossil calibrations. Supplementary Data 8: Metadata for all specimens and wild-caught birds used for morphological measurements of the beak and wing. Specimens are listed alphabetically by species. A forthcoming database publication led by J.A.T. will include morphological measurements by specimen

  4. Supplementary Table 9

    Multi-model inference of predictor effects for sympatry versus parapatry of bird sister species in contact

  5. Supplementary Table 11

    Sensitivity analyses investigating predictor effects for contact versus absence of contact in bird sister species, from an alternate approach to phylogenetic inference and divergence time estimation

  6. Supplementary Table 13

    Sensitivity analyses investigating predictor effects for sympatry versus parapatry of bird sister species in contact, from an alternate approach to phylogenetic inference and divergence time estimation

About this article

Publication history