Multiple routes to mammalian diversity

Journal name:
Nature
Volume:
479,
Pages:
393–396
Date published:
DOI:
doi:10.1038/nature10516
Received
Accepted
Published online

The radiation of the mammals provides a 165-million-year test case for evolutionary theories of how species occupy and then fill ecological niches. It is widely assumed that species often diverge rapidly early in their evolution, and that this is followed by a longer, drawn-out period of slower evolutionary fine-tuning as natural selection fits organisms into an increasingly occupied niche space1, 2. But recent studies have hinted that the process may not be so simple3, 4, 5. Here we apply statistical methods that automatically detect temporal shifts in the rate of evolution through time to a comprehensive mammalian phylogeny6 and data set7 of body sizes of 3,185 extant species. Unexpectedly, the majority of mammal species, including two of the most speciose orders (Rodentia and Chiroptera), have no history of substantial and sustained increases in the rates of evolution. Instead, a subset of the mammals has experienced an explosive increase (between 10- and 52-fold) in the rate of evolution along the single branch leading to the common ancestor of their monophyletic group (for example Chiroptera), followed by a quick return to lower or background levels. The remaining species are a taxonomically diverse assemblage showing a significant, sustained increase or decrease in their rates of evolution. These results necessarily decouple morphological diversification from speciation and suggest that the processes that give rise to the morphological diversity of a class of animals are far more free to vary than previously considered. Niches do not seem to fill up, and diversity seems to arise whenever, wherever and at whatever rate it is advantageous.

At a glance

Figures

  1. Log-likelihood of trait models when rates are allowed to vary.
    Figure 1: Log-likelihood of trait models when rates are allowed to vary.

    a, Posterior distribution of log-likelihoods from a model with equal rates of evolution (red), compared with the posterior distribution of log-likelihoods from the model in which evolutionary rates are allowed to vary (green): log(Bayes factor) = 993.51 (calculated from the log-harmonic means of the likelihoods); values >10 considered ‘very strong’ support. b, The coloured bars show distributions of rates for the one-third of the branches (1,494) for which the posterior probability of having a rate shift was greater than 0.95. Blue bars signify x-fold rate increases and yellow bars indicate x-fold rate decreases. Grey bars show the distribution of the mean fold rates for all the branches in the mammal phylogeny, independent of the level of posterior support.

  2. Rates of mammalian morphological evolution through time.
    Figure 2: Rates of mammalian morphological evolution through time.

    a, Mean time-dependent rates of evolution for the mammalian radiation taken as a whole. b, Mean time-dependent rates of evolution within each mammalian order. The colour key matches that in the dated phylogeny in a (dates taken from the corrigendum to ref. 6), which has been collapsed to the level of order; the start of each triangle indicates the first split in that order. Orders shaded grey in the phylogeny have rates throughout their evolutionary history that fall within the grey bar in b. The mean rates presented in a and b are calculated taking in to account the shared ancestry as implied by the phylogeny (mean rate decreases are less than one).

  3. The mammalian phylogenetic tree scaled to reflect morphological evolution.
    Figure 3: The mammalian phylogenetic tree scaled to reflect morphological evolution.

    The branches of the phylogeny are transformed by the mean of the posterior distribution of the scalars acting on each branch—the branches of the tree are stretched and compressed to reflect the rate of morphological evolution. Also, the branches are coloured according to how much they have been scaled (scale factor shown in colour bar).

References

  1. Simpson, G. G. Tempo and Mode in Evolution (Columbia Univ. Press, 1944)
  2. Foote, M. Morphological disparity in Ordovician-Devonian crinoids and the early saturation of morphological space. Paleobiology 20, 320344 (1994)
  3. Harmon, L. J. et al. Early bursts of body size and shape evolution are rare in comparative data. Evolution 64, 23852396 (2010)
  4. Cooper, N. & Purvis, A. Body size evolution in mammals: complexity in tempo and mode. Am. Nat. 175, 727738 (2010)
  5. Clauset, A. & Erwin, D. H. Evolution and distribution of species body size. Science 321, 399401 (2008)
  6. Bininda-Emonds, O. R. P. et al. The delayed rise of present-day mammals. Nature 446, 507512 (2007); corrigendum. 456, 274 (2008)
  7. Jones, K. E. et al. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90, 2648 (2009)
  8. Pagel, M. Inferring evolutionary processes from phylogenies. Zool. Scr. 26, 331348 (1997)
  9. Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877884 (1999)
  10. Green, P. J. Reversible jump Markov chain Monte Carlo computation and Bayesian model determination. Biometrika 82, 711732 (1995)
  11. Raftery, A. E. in Markov Chain Monte Carlo in Practice (eds Gilks, W. R., Richardson, S. & Spiegelhalter, D. J.) 163187 (Chapman & Hall, 1996)
  12. Read, A. F. & Harvey, P. H. Life history differences among the eutherian radiations. J. Zool. 219, 329353 (1989)
  13. Foote, M. Evolutionary patterns in the fossil record. Evolution 50, 111 (1996)
  14. Simpson, G. G. The Major Features of Evolution (Columbia Univ. Press, 1953)
  15. Clauset, A. & Redner, S. Evolutionary model of species body mass diversification. Phys. Rev. Lett. 102, 038103 (2009)
  16. Alroy, J. Cope’s rule and the dynamics of body mass evolution in North American Fossil mammals. Science 280, 731734 (1998)
  17. Smith, F. A., Betancourt, J. L. & Brown, J. H. Evolution of body size in the woodrat over the past 25,000 years of climate change. Science 270, 20122014 (1995)
  18. Smith, F. A., Browning, H. & Shepherd, U. L. The influence of climate change on the body mass of woodrats Neotoma in an arid region of New Mexico, USA. Ecography 21, 140148 (1998)
  19. Pollard, K. S. et al. An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443, 167172 (2006)
  20. Slater, G. J., Price, S. A., Santini, F. & Alfaro, M. E. Diversity versus disparity and the radiation of modern cetaceans. Proc. R. Soc. Lond. B 277, 30973104 (2010)
  21. Gingerich, P. D. Evolution and the fossil record: patterns, rates, and processes. Can. J. Zool. 65, 10531060 (1987)
  22. Hunt, G. Fitting and comparing models of phyletic evolution: random walks and beyond. Paleobiology 32, 578601 (2006)
  23. Polly, P. D. Paleontology and the comparative method: ancestral node reconstructions versus observed node values. Am. Nat. 157, 596609 (2001)
  24. Ruta, M., Wagner, P. J. & Coates, M. I. Evolutionary patterns in early tetrapods. I. Rapid initial diversification followed by decrease in rates of character change. Proc. R. Soc. Lond. B 273, 21072111 (2006)
  25. Venditti, C., Meade, A. & Pagel, M. Phylogenies reveal new interpretation of speciation and the Red Queen. Nature 463, 349352 (2010)

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Author information

Affiliations

  1. Department of Biological Sciences, University of Hull, Hull HU6 7RX, UK

    • Chris Venditti
  2. School of Biological Sciences, University of Reading, Reading RG6 6BX, UK

    • Andrew Meade &
    • Mark Pagel
  3. Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, New Mexico 87501, USA

    • Mark Pagel

Contributions

C.V., A.M. and M.P. contributed to all aspects of this work.

Competing financial interests

The authors declare no competing financial interests.

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Supplementary information

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  1. Supplementary Information (799K)

    The file contains Supplementary Figures 1-14 with legends, Supplementary Text and additional references.

Comments

  1. Report this comment #28602

    Ido Pen said:

    Very nice analysis, but the final paragraph of the paper is a bit too speculative in my opinion. For example, how does it follow from the analysis that "natural selection has found multiple different routes to producing the current diversity of sizes."? I don't see how a role for natural selection has been established.

  2. Report this comment #30510

    Nathan Jeffery said:

    Morphology (syn. form) pertains to shape as well as size. Statements like "...necessarily decouple morphological diversification from speciation..." are a little ambiguous and should only refer to body size. Palaeontologists and alike also spend a considerable amount of time documenting and analysing the diversification of shape in relation to speciation.

  3. Report this comment #32764

    Derek Yalden said:

    While this is an interesting analysis, it is also very misleading (and that is quite apart from reassigning Taphozous to the Megachiroptera – presumably Pteropus was intended). Major morphological changes, such as the loss of hind limbs in Cetacea and Sirenia, seem not to show the pattern here, which only considers size changes and should not attempt to conceal that. In any case, the assumption of a burst of evolutionary divergence at the K-T boundary usually implies numerical diversity, not size change, as the critical change. So this analysis puzzles me more than it enlightens.

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