Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Phylogenetic evidence for mid-Cenozoic turnover of a diverse continental biota

Nature Ecology & Evolution volume 1, pages 1896–1902 (2017)Cite this article

Subjects

Abstract

Rapid climatic change at the beginning of the Oligocene epoch is concordant with global biotic turnover in the fossil record. However, while Southern Hemisphere geological movement played a key role in shaping these global climatic shifts, given generally poor terrestrial fossil records, evidence for matching turnover in entire Austral biotas is lacking. Emerging comprehensive phylogenetic frameworks provide alternative avenues to explore for signals of mass turnover or restructuring. Here, we combine phylogenetic data with empirical and simulation-based approaches to understand the temporal dynamics of the origins of a diverse and highly endemic continental biota (Australian lizards and snakes). These analyses indicate that the temporal clustering of major radiation ages in Gondwanan endemic lineages and immigration into Australia is narrower than expected under time-continuous models assuming no overarching external perturbation. Independent phylogenetic dating analyses further indicate that the timing of both processes is concentrated in the period post-dating the Eocene–Oligocene transition (~34 million years ago). Epoch-defining processes around the start of the Oligocene appear to have also played a decisive role in reshaping a diverse Southern Hemisphere biota—by both re-setting Gondwanan endemic diversity and opening the way to successful immigration from the north.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Phylogenetic position, age and origins of Australian squamates.

images: Mark Hutchinson (elapids, pythons, blindsnake, Eugongylus group, Sphenomorphus group and Ctenotus); Brad Maryan (Varanus, Crenadactylus and Pygopodidae); Paul Oliver (Gehyra and Agamids); and Juniors Bildarchiv GmbH/Alamy Stock Photo (Egernia).

Fig. 2: Crown and stem ages for extant Australian squamate groups.
Fig. 3: Maximum likelihood ancestral states and time-dependent BiSSE analyses of immigration into Australia.
Fig. 4: Observed versus expected temporal spread (s.d./mean) of crown ages for Australian lineages given the length of time they have been present in Australia.

Similar content being viewed by others

References

  1. Jablonski, D. Mass extinctions and macroevolution. Paleobiology 31, 192–210 (2005).

    Article  Google Scholar 

  2. Schulte, P. et al. The Chicxulub asteroid impact and mass extinction at the Cretaceous–Paleogene boundary. Science 327, 1214–1218 (2010).

    Article  CAS  PubMed  Google Scholar 

  3. Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Raup, D. & Sepkoski, J. J. Periodic extinction of families and genera. Science 231, 833–836 (1986).

    Article  CAS  PubMed  Google Scholar 

  5. Hooker, J. J., Collinson, M. E. & Sille, N. P. Eocene–Oligocene mammalian faunal turnover in the Hampshire Basin, UK: calibration to the global time scale and the major cooling event. J. Geol. Soc. Lond. 161, 161–172 (2004).

    Article  Google Scholar 

  6. Augé, M. & Smith, R. An assemblage of early Oligocene lizards (Squamata) from the locality of Boutersem (Belgium), with comments on the Eocene–Oligocene transition. Zool. J. Linn. Soc. 155, 148–170 (2009).

    Article  Google Scholar 

  7. Sun, J. et al. Synchronous turnover of flora, fauna, and climate at the Eocene–Oligocene boundary in Asia. Sci. Rep. 4, 7463 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. McGowran, B., Holdgate, G. R., Li, Q. & Gallagher, S. J. Cenozoic stratigraphic succession in southeastern Australia. Aust. J. Earth Sci. 51, 459–496 (2004).

    Article  Google Scholar 

  9. Jarvis, E. D. et al. Whole genome analyses resolve the early branches in the tree of life of modern birds. Science 346, 1320–1331 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Meredith, R. W. et al. Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334, 521–524 (2011).

    Article  CAS  PubMed  Google Scholar 

  11. Feng, Y.-J. et al. Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous–Paleogene boundary. Proc. Natl Acad. Sci. USA 114, E5864–E5870 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Stadler, T. Mammalian phylogeny reveals recent diversification rate shifts. Proc. Natl Acad. Sci. USA 108, 6187–6192 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Crisp, M. D. & Cook, L. G. Explosive radiation or cryptic mass extinction? Interpreting signatures in molecular phylogenies. Evolution 63, 2257–2265 (2009).

    Article  PubMed  Google Scholar 

  14. Hall, R. Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer based reconstructions, model and animations. J. Asian Earth Sci. 20, 353–431 (2002).

    Article  Google Scholar 

  15. Lawver, L. A. & Gahagan, L. M. Evolution of Cenozoic seaways in the circum-Antarctic region. Palaeogeogr. Palaeoclimatol. Palaeoecol. 198, 11–37 (2003).

    Article  Google Scholar 

  16. Scher, H. D. et al. Onset of Antarctic circumpolar current 30 million years ago as Tasmanian Gateway aligned with westerlies. Nature 523, 580–583 (2015).

    Article  CAS  PubMed  Google Scholar 

  17. Rabosky, D. L. Challenges in the estimation of extinction from molecular phylogenies: a response to Beaulieu and O’Meara. Evolution 70, 218–228 (2016).

    Article  PubMed  Google Scholar 

  18. Beaulieu, J. M. & O’Meara, B. C. Extinction can be estimated from moderately sized molecular phylogenies. Evolution 69, 1036–1043 (2015).

    Article  PubMed  Google Scholar 

  19. Wilson, S. & Swan, G. A Complete Guide to Reptiles of Australia 5th edn (New Holland, Sydney, 2017).

  20. Keast, A. (ed.) Ecological Biogeography of Australia (Springer, Dordrecht, 1981).

  21. Brennan, I. G. & Oliver, P. M. Mass turnover and recovery dynamics of a diverse Australian continental radiation. Evolution 71, 1352–1365 (2017).

    Article  PubMed  Google Scholar 

  22. Oliver, P. M. & Bauer, A. M. Systematics and evolution of the Australian knob-tail geckos (Nephrurus, Carphodactylidae, Gekkota): plesiomorphic grades and biome shifts through the Miocene. Mol. Phylogenet. Evol. 59, 664–674 (2011).

    Article  PubMed  Google Scholar 

  23. Oliver, P. M. & Sanders, K. L. Molecular evidence for Gondwanan origins of multiple lineages within a diverse Australasian gecko radiation. J. Biogeogr. 36, 2044–2055 (2009).

    Article  Google Scholar 

  24. Oliver, P. M., Adams, M. & Doughty, P. Molecular evidence for ten species and Oligo–Miocene vicariance within a nominal Australian gecko species (Crenadactylus ocellatus, Diplodactylidae). BMC Evol. Biol. 10, 386 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Skinner, A., Hugall, A. F. & Hutchinson, M. N. Lygosomine phylogeny and the origins of Australian scincid lizards. J. Biogeogr. 38, 1044–1058 (2011).

    Article  Google Scholar 

  26. Chen, I., Stuart-fox, D., Hugall, A. F. & Symonds, M. R. E. Sexual selection and the evolution of complex color patterns in dragon lizards. Evolution 66, 3605–3614 (2012).

    Article  PubMed  Google Scholar 

  27. Heinicke, M. P., Greenbaum, E., Jackman, T. R. & Bauer, A. M. Phylogeny of a trans-Wallacean radiation (Squamata, Gekkonidae, Gehyra) supports a single early colonization of Australia. Zool. Scr. 40, 584–602 (2011).

    Article  Google Scholar 

  28. Vidal, N. et al. Molecular evidence for an Asian origin of monitor lizards followed by tertiary dispersals to Africa and Australasia. Biol. Lett. 8, 853–855 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Vidal, N. et al. Blindsnake evolutionary tree reveals long history on Gondwana. Biol. Lett. 6, 558–561 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Sanders, K. L., Lee, M. S. Y., Leys, R., Foster, R. & Keogh, J. S. Molecular phylogeny and divergence dates for Australasian elapids and sea snakes (Hydrophiinae): evidence from seven genes for rapid evolutionary radiations. J. Evol. Biol. 21, 682–695 (2008).

    Article  CAS  PubMed  Google Scholar 

  31. Scanlon, J. D. & Lee, M. S. Y. in Reproductive Biology and Phylogeny of Snakes (eds Sever, D. & Aldridge, R.) 55–95 (CRC, Boca Raton, 2010).

  32. Pyron, R. A., Burbrink, F. T. & Wiens, J. J. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13, 93 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Hartmann, K., Wong, D. & Stadler, T. Sampling trees from evolutionary models. Syst. Biol. 59, 465–476 (2010).

    Article  PubMed  Google Scholar 

  34. Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    Article  CAS  PubMed  Google Scholar 

  35. Fitzjohn, R. G. Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3, 1084–1092 (2012).

    Article  Google Scholar 

  36. Schumacher, S. & Lazarus, D. Regional differences in pelagic productivity in the late Eocene to early Oligocene—a comparison of southern high latitudes and lower latitudes. Palaeogeogr. Palaeoclimatol. Palaeoecol. 214, 243–263 (2004).

    Article  Google Scholar 

  37. Byrne, M. et al. Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota. Mol. Ecol. 17, 4398–4417 (2008).

    Article  CAS  PubMed  Google Scholar 

  38. Byrne, M. et al. Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. J. Biogeogr. 38, 1635–1656 (2011).

    Article  Google Scholar 

  39. Hooker, J. D. in Botany of the Antarctic Voyage of H.M. Discovery Ships Erebus and Terror in the Years 1839–1843, III. Flora Tasmaniae (ed. Hooker, J. D.) 1–36 (Reeve, London, 1860).

  40. Crisp, M. D. & Cook, L. G. How was the Australian flora assembled over the last 65 million years? A molecular phylogenetic perspective. Annu. Rev. Ecol. Evol. Syst. 44, 303–324 (2013).

    Article  Google Scholar 

  41. Powney, G. D., Grenyer, R., Orme, C. D. L., Owens, I. P. F. & Meiri, S. Hot, dry and different: Australian lizard richness is unlike that of mammals, amphibians and birds. Glob. Ecol. Biogeogr. 19, 386–396 (2010).

    Article  Google Scholar 

  42. Mitchell, K. J. et al. Molecular phylogeny, biogeography, and habitat preference evolution of marsupials. Mol. Biol. Evol. 31, 2322–2330 (2014).

    Article  CAS  PubMed  Google Scholar 

  43. Schweizer, M., Seehausen, O. & Hertwig, S. T. Macroevolutionary patterns in the diversification of parrots: effects of climate change, geological events and key innovations. J. Biogeogr. 38, 2176–2194 (2011).

    Article  Google Scholar 

  44. Sniderman, J. M. K. & Jordan, G. J. Extent and timing of floristic exchange between Australian and Asian rain forests. J. Biogeogr. 38, 1445–1455 (2011).

    Article  Google Scholar 

  45. Maekawa, K., Lo, N., Rose, H. A. & Matsumoto, T. The evolution of soil-burrowing cockroaches (Blattaria: Blaberidae) from wood-burrowing ancestors following an invasion of the latter from Asia into Australia. Proc. R. Soc. Lond. B 270, 1301–1307 (2003).

    Article  Google Scholar 

  46. Hugall, A. F. & Stanisic, J. Beyond the prolegomenon: a molecular phylogeny of the Australian camaenid land snail radiation. Zool. J. Linn. Soc. 161, 531–572 (2011).

    Article  Google Scholar 

  47. Kurabayashi, A. et al. From Antarctica or Asia? New colonization scenario for Australian–New Guinean narrow mouth toads suggested from the findings on a mysterious genus Gastrophrynoides. BMC Evol. Biol. 11, 175 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Jønsson, K. A., Fabre, P., Ricklefs, R. E. & Fjeldså, J. Major global radiation of corvoid birds originated in the proto-Papuan archipelago. Proc. Natl Acad. Sci. USA 108, 2328–2333 (2010).

    Article  Google Scholar 

  49. Brandley, M. C. et al. Accommodating heterogenous rates of evolution in molecular divergence dating methods: an example using intercontinental dispersal of plestiodon (Eumeces) lizards. Syst. Biol. 60, 3–15 (2011).

    Article  CAS  PubMed  Google Scholar 

  50. Stamatakis, A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006).

    Article  CAS  PubMed  Google Scholar 

  51. Ronquist, F. et al. Mrbayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Drummond, A. J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Sanderson, M. J. Evolution and divergence times in the absence of a molecular clock. Evolution 19, 301–302 (2003).

    CAS  Google Scholar 

  54. Foster, C. S. P. et al. Evaluating the impact of genomic data and priors on Bayesian estimates of the angiosperm evolutionary timescale. Syst. Biol. 66, 338–351 (2017).

    PubMed  Google Scholar 

  55. Britton, T., Oxelman, B., Vinnersten, A. & Bremer, K. Phylogenetic dating with confidence intervals using mean path lengths. Mol. Phylogenet. Evol. 24, 58–65 (2002).

    Article  CAS  PubMed  Google Scholar 

  56. McGuire, J. A. et al. Molecular phylogenetics and the diversification of hummingbirds. Curr. Biol. 24, 910–916 (2014).

    Article  CAS  PubMed  Google Scholar 

  57. Rabosky, D. L. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9, e89543 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Crisp, M. D. & Cook, L. G. A congruent molecular signature of vicariance across multiple plant lineages. Mol. Phylogenet. Evol. 43, 1106–1117 (2007).

    Article  CAS  PubMed  Google Scholar 

  59. Hickerson, M. J., Stahl, E. A. & Lessios, H. A. Test for simultaneous divergence using approximate Bayesian computation. Evolution 60, 2435–2453 (2006).

    Article  CAS  PubMed  Google Scholar 

  60. Near, T. J. et al. Boom and bust: ancient and recent diversification in bichirs (Polypteridae: Actinopterygii), a relictual lineage of ray-finned fishes. Evolution 68, 1014–1026 (2014).

    Article  PubMed  Google Scholar 

  61. Magallón, S. & Sanderson, M. J. Absolute diversification rates in angiosperm clades. Evolution 55, 1762–1780 (2001).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

P.M.O. was supported by a McKenzie Postdoctoral Fellowship from the University of Melbourne and an Australian Reseach Council Early Career Researcher Fellowship. We thank L. Bromham, M. Cardillo, M. Novosolov and C. Moritz for comments.

Author information

Authors and Affiliations

  1. Research School of Biology and Centre for Biodiversity Analysis, Australian National University, Canberra, Australian Capital Territory, 0200, Australia

    Paul M. Oliver

  2. Department of Sciences, Museums Victoria, Melbourne, Victoria, 3001, Australia

    Andrew F. Hugall

Authors
  1. Paul M. Oliver
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrew F. Hugall
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

P.M.O. and A.F.H. conceived the project, undertook the analyses and wrote the paper.

Corresponding author

Correspondence to Paul M. Oliver.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

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

Electronic supplementary material

Supplementary Information

Supplementary Notes 1-3, Supplementary Tables 1-6, Supplementary Figures 1-3

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oliver, P.M., Hugall, A.F. Phylogenetic evidence for mid-Cenozoic turnover of a diverse continental biota. Nat Ecol Evol 1, 1896–1902 (2017). https://doi.org/10.1038/s41559-017-0355-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-017-0355-8

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing