Letter | Published:

Species coexistence and the dynamics of phenotypic evolution in adaptive radiation

Nature volume 506, pages 359363 (20 February 2014) | Download Citation

Subjects

Abstract

Interactions between species can promote evolutionary divergence of ecological traits and social signals1,2, a process widely assumed to generate species differences in adaptive radiation3,4,5. However, an alternative view is that lineages typically interact when relatively old6, by which time selection for divergence is weak7,8 and potentially exceeded by convergent selection acting on traits mediating interspecific competition9. Few studies have tested these contrasting predictions across large radiations, or by controlling for evolutionary time. Thus the role of species interactions in driving broad-scale patterns of trait divergence is unclear10. Here we use phylogenetic estimates of divergence times to show that increased trait differences among coexisting lineages of ovenbirds (Furnariidae) are explained by their greater evolutionary age in relation to non-interacting lineages, and that—when these temporal biases are accounted for—the only significant effect of coexistence is convergence in a social signal (song). Our results conflict with the conventional view that coexistence promotes trait divergence among co-occurring organisms at macroevolutionary scales, and instead provide evidence that species interactions can drive phenotypic convergence across entire radiations, a pattern generally concealed by biases in age.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Accessions

Data deposits

Nuclear and mitochondrial DNA sequences for all lineages have been deposited in GenBank under accession numbers given in Supplementary Data 1.

References

  1. 1.

    & Evolution of character displacement in Darwin’s finches. Science 313, 224–226 (2006)

  2. 2.

    & Songs of Darwin’s finches diverge when a new species enters the community. Proc. Natl Acad. Sci. USA 107, 20156–20163 (2010)

  3. 3.

    On the Origin of Species (John Murray, 1859)

  4. 4.

    Tempo and Mode in Evolution (Columbia Univ. Press, 1944)

  5. 5.

    & Character displacement and the origins of diversity. Am. Nat. 176, S26–S44 (2010)

  6. 6.

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

  7. 7.

    The roles of time and ecology in the continental radiation of the Old World leaf warblers (Phylloscopus and Seicercus). Phil. Trans. R. Soc. B 365, 1749–1762 (2010)

  8. 8.

    & Character displacement from the receiver’s perspective: species and mate recognition despite convergent signals in suboscine birds. Proc. R. Soc. Lond. B 277, 2475–2483 (2010)

  9. 9.

    , , & The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol. Rev. Camb. Philos. Soc. 84, 617–635 (2009)

  10. 10.

    & Darwin’s bridge between microevolution and macroevolution. Nature 457, 837–842 (2009)

  11. 11.

    & Character displacement. Syst. Zool. 5, 49–64 (1956)

  12. 12.

    & Character displacement: ecological and reproductive responses to a common evolutionary problem. Q. Rev. Biol. 84, 253–276 (2009)

  13. 13.

    & Adaptive radiation: contrasting theory with data. Science 323, 732–737 (2009)

  14. 14.

    & Ecological and community-wide character displacement: the next generation. Ecol. Lett. 8, 875–894 (2005)

  15. 15.

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

  16. 16.

    et al. A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387, 589–592 (1997)

  17. 17.

    , , & Species co-existence and character divergence across carnivores. Ecol. Lett. 10, 146–152 (2007)

  18. 18.

    Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35, 131–138 (1980)

  19. 19.

    & Adaptive radiation, non-adaptive radiation, ecological speciation and non-ecological speciation. Trends Ecol. Evol. 24, 394–399 (2009)

  20. 20.

    et al. Lineage diversification and morphological evolution in a large-scale continental radiation: the Neotropical ovenbirds and woodcreepers (Aves: Furnariidae). Evolution 65, 2973–2986 (2011)

  21. 21.

    Ecological adaptation and species recognition drive vocal evolution in Neotropical suboscine birds. Evolution 59, 200–215 (2005)

  22. 22.

    et al. Song divergence by sensory drive in Amazonian birds. Evolution 64, 2820–2839 (2010)

  23. 23.

    et al. Correlated evolution of beak morphology and song in the Neotropical woodcreeper radiation. Evolution 66, 2784–2797 (2012)

  24. 24.

    et al. Testing limiting similarity in Quaternary terrestrial gastropods. Paleobiology 34, 378–388 (2008)

  25. 25.

    Does competition drive character differences between species on a macroevolutionary scale? J. Evol. Biol. 25, 2341–2347 (2012)

  26. 26.

    & Species interactions constrain geographic range expansion over evolutionary time. Ecol. Lett. 16, 330–338 (2012)

  27. 27.

    & Signal design and perception in Hypocnemis antbirds: evidence for convergent evolution via social selection. Evolution 63, 3168–3189 (2009)

  28. 28.

    Interspecific interactions drive cultural co-evolution and acoustic convergence in syntopic species. J. Anim. Ecol. 81, 594–604 (2012)

  29. 29.

    , & The role of ecological constraint in driving the evolution of avian song frequency across a latitudinal gradient. Evolution 66, 2773–2783 (2012)

  30. 30.

    , & Convergent evolution within an adaptive radiation of cichlid fishes. Curr. Biol. 22, 2362–2368 (2012)

  31. 31.

    et al. Digital Distribution Maps of the Birds of the Western Hemisphere, v. 2.1 (NatureServe, 2005)

  32. 32.

    & Mode of speciation in birds: a test of Lynch’s method. Evolution 48, 490–497 (1995)

  33. 33.

    in Speciation and its Consequences (eds & ) 527–553 (Sinauer, 1989)

  34. 34.

    & Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53, 983–997 (1997)

  35. 35.

    & Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under nonstandard conditions. J. Am. Stat. Assoc. 82, 605–610 (1987)

  36. 36.

    , , , & ASReml User Guide, Release 3.0 (VSN International, 2009)

  37. 37.

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

  38. 38.

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

  39. 39.

    , , & Package nlme: Linear and Nonlinear Mixed Effects Models, v. 3.1-109 (R-core, 2013)

  40. 40.

    , , , & GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129–131 (2008)

Download references

Acknowledgements

We thank G. Grether, J. Hadfield, S. Nakagawa, A. Phillimore, A. Pigot, R. Ricklefs, G. Thomas and S. West for comments and discussion. We are also indebted to the many individuals who collected specimens, tissue samples and sound recordings, and to numerous institutions (particularly the Macaulay Library, Cornell University) for granting access to this material. Complete acknowledgements and data sets are provided in the Supplementary Information. This research was supported by the John Fell Fund (to J.A.T.), the Browne Fellowship, Queen’s College, Oxford, and Vetenskapsrådet (to C.K.C.), the National Science Foundation (to R.T.B.) and the Royal Society (to N.S.).

Author information

Author notes

    • Joseph A. Tobias
    •  & Charlie K. Cornwallis

    These authors contributed equally to this study.

Affiliations

  1. Edward Grey Institute, Department of Zoology, University of Oxford, Oxford OX1 3PS, UK

    • Joseph A. Tobias
    • , Charlie K. Cornwallis
    •  & Nathalie Seddon
  2. Department of Biology, Lund University, Lund, SE-223 62, Sweden

    • Charlie K. Cornwallis
  3. Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana 70803, USA

    • Elizabeth P. Derryberry
    • , Santiago Claramunt
    •  & Robb T. Brumfield
  4. Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, Louisiana 70118, USA

    • Elizabeth P. Derryberry
  5. Museum of Natural Science, Louisiana State University, Baton Rouge, Louisiana 70803, USA

    • Santiago Claramunt
    •  & Robb T. Brumfield
  6. Department of Ornithology, American Museum of Natural History, New York, New York 10024, USA

    • Santiago Claramunt

Authors

  1. Search for Joseph A. Tobias in:

  2. Search for Charlie K. Cornwallis in:

  3. Search for Elizabeth P. Derryberry in:

  4. Search for Santiago Claramunt in:

  5. Search for Robb T. Brumfield in:

  6. Search for Nathalie Seddon in:

Contributions

J.A.T. and N.S. conceived and designed the study, compiled and analysed song data, and integrated all data sets; S.C. provided morphometric data; E.P.D., S.C. and R.T.B. conducted molecular sequencing and phylogenetic analyses; C.C. designed and conducted statistical analyses, with significant input from N.S.; N.S., J.A.T. and C.C. produced figures and tables; J.A.T. prepared and edited the manuscript, with input from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Joseph A. Tobias.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Methods, Supplementary Tables 1-27, a Supplementary Discussion, Supplementary Notes, Supplementary References and a Supplementary Code for Statistical Analyses.

Excel files

  1. 1.

    Supplementary Data

    The file contains Supplementary Datasets 1-7 – see file for details.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature12874

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.