Article | Published:

The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life

Nature Ecology & Evolutionvolume 2pages850858 (2018) | Download Citation

Abstract

Human activities continue to erode the tree of life, requiring us to prioritize research and conservation. Amphibians represent key victims and bellwethers of global change, and the need for action to conserve them is drastically outpacing knowledge. We provide a phylogeny incorporating nearly all extant amphibians (7,238 species). Current amphibian diversity is composed of both older, depauperate lineages and extensive, more recent tropical radiations found in select clades. Frog and salamander diversification increased strongly after the Cretaceous–Palaeogene boundary, preceded by a potential mass-extinction event in salamanders. Diversification rates of subterranean caecilians varied little over time. Biogeographically, the Afro- and Neotropics harbour a particularly high proportion of Gondwanan relicts, comprising species with high evolutionary distinctiveness (ED). These high-ED species represent a large portion of the branches in the present tree: around 28% of all phylogenetic diversity comes from species in the top 10% of ED. The association between ED and imperilment is weak, but many species with high ED are now imperilled or lack formal threat status, suggesting opportunities for integrating evolutionary position and phylogenetic heritage in addressing the current extinction crisis. By providing a phylogenetic estimate for extant amphibians and identifying their threats and ED, we offer a preliminary basis for a quantitatively informed global approach to conserving the amphibian tree of life.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Additional information

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

References

  1. 1.

    Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).

  2. 2.

    Dirzo, R. et al. Defaunation in the Anthropocene. Science 345, 401–406 (2014)

  3. 3.

    Bottrill, M. C. et al. Is conservation triage just smart decision making? Trends Ecol. Evol. 23, 649–654 (2008).

  4. 4.

    Conde, D. A. et al. Opportunities and costs for preventing vertebrate extinctions. Curr. Biol. 25, R219–R221 2015).

  5. 5.

    Purvis, A. & Hector, A. Getting the measure of biodiversity. Nature 405, 212–219 (2000).

  6. 6.

    Dawson, T. P., Jackson, S. T., House, J. I., Prentice, I. C. & Mace, G. M. Beyond predictions: biodiversity conservation in a changing climate. Science 332, 53–58 (2011).

  7. 7.

    Mace, G. M., Gittleman, J. L. & Purvis, A. Preserving the tree of life. Science 300, 1707–1709 (2003).

  8. 8.

    Vane-Wright, R. I., Humphries, C. J. & Williams, P. H. What to protect?—Systematics and the agony of choice. Biol. Conserv. 55, 235–254 (1991).

  9. 9.

    Faith, D. P. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 (1992).

  10. 10.

    Jetz, W. et al. Distribution and conservation of global evolutionary distinctness in birds. Curr. Biol. 24, 919–930 2014).

  11. 11.

    Isaac, N. J. B., Turvey, S. T., Collen, B., Waterman, C. & Baillie, J. E. M. Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLoS ONE 2, e296 (2007).

  12. 12.

    Rosauer, D. F. & Mooers, A. O.Nurturing the use of evolutionary diversity in nature conservation. Trends Ecol. Evol. 28, 322–323 2013).

  13. 13.

    Winter, M., Devictor, V. & Schweiger, O. Phylogenetic diversity and nature conservation: where are we? Trends Ecol. Evol. 28, 199–204 (2013).

  14. 14.

    Jetz, W. & Freckleton, R. P. Towards a general framework for predicting threat status of data-deficient species from phylogenetic, spatial and environmental information. Phil. Trans. R. Soc. B 370, 20140016 (2015).

  15. 15.

    Beebee, T. J. & Griffiths, R. A. The amphibian decline crisis: a watershed for conservation biology? Biol. Conserv. 125, 271–285 (2005).

  16. 16.

    Blaustein, A. R. & Kiesecker, J. M. Complexity in conservation: lessons from the global decline of amphibian populations. Ecol. Lett. 5, 597–608 (2002).

  17. 17.

    Pounds, A. J. et al. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161–167 (2006).

  18. 18.

    Mendelson, J. R. et al. Confronting amphibian declines and extinctions. Science 313, 48 (2006).

  19. 19.

    Stuart, S. N. et al. Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786 (2004).

  20. 20.

    Wake, D. B. & Vredenburg, V. T. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Natl Acad. Sci. USA 105, 11466–11473 (2008).

  21. 21.

    Houlahan, J. E., Findlay, C. S., Schmidt, B. R., Meyer, A. H. & Kuzmin, S. L. Quantitative evidence for global amphibian population declines. Nature 404, 752–755 (2000).

  22. 22.

    Blaustein, A. R. & Dobson, A. Extinctions: a message from the frogs. Nature 439, 143–144 (2006).

  23. 23.

    Sodhi, N. S. et al. Measuring the meltdown: drivers of global amphibian extinction and decline. PLoS ONE 3, e1636 (2008).

  24. 24.

    Brühl, C. A., Schmidt, T., Pieper, S. & Alscher, A. Terrestrial pesticide exposure of amphibians: an underestimated cause of global decline? Sci. Rep. 3, 1135 (2013).

  25. 25.

    Frost, D. R. et al. The amphibian tree of life. Bull. Am. Mus. Nat. Hist. 287, 1–291 (2006).

  26. 26.

    San Mauro, D., Vences, M., Alcobendas, M., Zardoya, R. & Meyer, A. Initial diversification of living amphibians predated the breakup of Pangaea. Am. Nat. 165, 590–599 (2005).

  27. 27.

    Benton, M. J. The Fossil Record 2 (Chapman & Hall, London, 1993).

  28. 28.

    Roelants, K. et al. Global patterns of diversification in the history of modern amphibians. Proc. Natl Acad. Sci. USA 104, 887–892 (2007).

  29. 29.

    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).

  30. 30.

    Redding, D. W. & Mooers, A. O. Incorporating evolutionary measures into conservation prioritization. Conserv. Biol. 20, 1670–1678 (2006).

  31. 31.

    Isaac, N. J. B., Redding, D. W., Meredith, H. M. & Safi, K. Phylogenetically-informed priorities for amphibian conservation. PLoS ONE 7, e43912 (2012).

  32. 32.

    An Analysis of Amphibians on the 2008 IUCN Red List (IUCN, Conservation International & NatureServe, 2008); http://www.iucnredlist.org/initiatives/amphibians

  33. 33.

    Blaustein, A. R. et al. Amphibian breeding and climate change. Conserv. Biol. 15, 1804–1809 (2001).

  34. 34.

    Hof, C., Araujo, M. B., Jetz, W. & Rahbek, C. Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nature 480, 516–519 (2011).

  35. 35.

    Yap, T. A., Koo, M. S., Ambrose, R. F., Wake, D. B. & Vredenburg, V. T. Averting a North American biodiversity crisis. Science 349, 481–482 (2015).

  36. 36.

    Lawler, J., Shafer, S., Bancroft, B. & Blaustein, A. Projected climate impacts for the amphibians of the Western Hemisphere. Conserv. Biol. 24, 38–50 (2010).

  37. 37.

    Buckley, L. B., Hurlbert, A. H. & Jetz, W. Broad-scale ecological implications of ectothermy and endothermy in changing environments. Glob. Ecol. Biogeogr. 21, 873–885 (2012).

  38. 38.

    Blaustein, A. R., Wake, D. B. & Sousa, W. P. Amphibian declines: judging stability, persistence, and susceptibility of populations to local and global extinctions. Conserv. Biol. 8, 60–71 (1994).

  39. 39.

    Vieites, D. R. et al. Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proc. Natl Acad. Sci. USA 106, 8267–8272 (2009).

  40. 40.

    Kohler, J. et al. New amphibians and global conservation: a boost in species discoveries in a highly endangered vertebrate group. Bioscience 55, 693–696 (2005).

  41. 41.

    Ficetola, G. F. et al. An evaluation of the robustness of global amphibian range maps. J. Biogeogr. 41, 211–221 (2014).

  42. 42.

    Meyer, C., Kreft, H., Guralnick, R. & Jetz, W. Global priorities for an effective information basis of biodiversity distributions. Nat. Commun. 6, 8221 (2015).

  43. 43.

    Meegaskumbura, M. et al. Sri Lanka: an amphibian hot spot. Science 298, 379 (2002).

  44. 44.

    Höhna, S. Fast simulation of reconstructed phylogenies under global time-dependent birth–death processes. Bioinformatics 29, 1367–1374 (2013).

  45. 45.

    Kozak, K. H., Weisrock, D. W. & Larson, A. Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon). Proc. R. Soc. B 273, 539–546 (2006).

  46. 46.

    Wu, Y. & Murphy, R. W. Concordant species delimitation from multiple independent evidence: a case study with the Pachytriton brevipes complex (Caudata: Salamandridae). Mol. Phylogenet. Evol. 92, 108–117 (2015).

  47. 47.

    May, M. R., Höhna, S. & Moore, B. R. A Bayesian approach for detecting the impact of mass-extinction events on molecular phylogenies when rates of lineage diversification may vary. Methods Ecol. Evol. 7, 947–959 (2016).

  48. 48.

    Springer, M. S. et al. Waking the undead: implications of a soft explosive model for the timing of placental mammal diversification. Mol. Phylogenet. Evol. 106, 86–102 (2017).

  49. 49.

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

  50. 50.

    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).

  51. 51.

    Pyron, R. A. Biogeographic analysis reveals ancient continental vicariance and recent oceanic dispersal in amphibians. Syst. Biol. 63, 779–797 (2014).

  52. 52.

    Safi, K., Armour-Marshall, K., Baillie, J. E. M. & Isaac, N. J. B. Global patterns of evolutionary distinct and globally endangered amphibians and mammals. PLoS ONE 8, e63582 (2013).

  53. 53.

    Fritz, S. A. & Rahbek, C.Global patterns of amphibian phylogenetic diversity. J. Biogeogr. 39, 1373–1382 (2012).

  54. 54.

    Buckley, L. & Jetz, W. Environmental and historical constraints on global patterns of amphibian richness. Proc. R. Soc. B 274, 1167–1173 (2007).

  55. 55.

    Buckley, L. B. & Jetz, W. Linking global turnover of species and environments. Proc. Natl Acad. Sci. USA 105, 17836–17841 (2008).

  56. 56.

    Pyron, R. A. & Wiens, J. J. Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diversity. Proc. R. Soc. B 280, 20131622 (2013).

  57. 57.

    Wiens, J. J. Global patterns of diversification and species richness in amphibians. Am. Nat. 170, S86–S106 (2007).

  58. 58.

    Steel, M., Mimoto, A. & Mooers, A. O. Hedging our bets: the expected contribution of species to future phylogenetic diversity. Evol. Bioinform. Online 3, 237–244 (2007).

  59. 59.

    Kerby, J. L., Richards-Hrdlicka, K. L., Storfer, A. & Skelly, D. K. An examination of amphibian sensitivity to environmental contaminants: are amphibians poor canaries? Ecol. Lett. 13, 60–67 (2010).

  60. 60.

    Schachat, S. R., Mulcahy, D. G. & Mendelson, J. R. Conservation threats and the phylogenetic utility of IUCN Red List rankings in Incilius toads. Conserv. Biol. 30, 72–81 (2016).

  61. 61.

    Thomas, G. H. et al. PASTIS: an R package to facilitate phylogenetic assembly with soft taxonomic inferences. Methods Ecol. Evol. 4, 1011–1017 (2013).

  62. 62.

    Barej, M. et al. Life in the spray zone—overlooked diversity in West African torrent-frogs (Anura, Odontobatrachidae, Odontobatrachus). Zoosyst. Evol. 91, 115–149 (2015).

  63. 63.

    Rabosky, D. L. No substitute for real data: a cautionary note on the use of phylogenies from birth–death polytomy resolvers for downstream comparative analyses. Evolution 69, 3207–3216 (2015).

  64. 64.

    Tonini, J. F. R., Beard, K. H., Ferreira, R. B., Jetz, W. & Pyron, R. A.Fully-sampled phylogenies of squamates reveal evolutionary patterns in threat status. Biol. Conserv. 204, 23–31 (2016).

  65. 65.

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

  66. 66.

    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).

  67. 67.

    Rabosky, D. L. No substitute for real data: a cautionary note on the use of phylogenies from birth–death polytomy resolvers for downstream comparative analyses. Evolution 69, 3207–3216 (2015).

  68. 68.

    Redding, D. W. Incorporating Genetic Distinctness and Reserve Occupancy Into a Conservation Priorisation Approach. MSc thesis, Univ. East Anglia (2003).

  69. 69.

    Redding, D. W., Mazel, F. & Mooers, A. Ø. Measuring evolutionary isolation for conservation. PLoS ONE 9, e113490 (2014).

  70. 70.

    Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).

  71. 71.

    Cadotte, M. W. & Davies, T. J. Rarest of the rare: advances in combining evolutionary distinctiveness and scarcity to inform conservation at biogeographical scales. Divers. Distrib. 16, 376–385 (2010).

  72. 72.

    Höhna, S., May, M. R. & Moore, B. R. Phylogeny Simulation and Diversification Rate Analysis with TESS (2015); https://cran.r-project.org/web/packages/TESS/vignettes/Bayesian_Diversification_Rate_Analysis.pdf

  73. 73.

    Threats Classification Scheme (Version 3.2) (IUCN, 2017); http://www.iucnredlist.org/technicaldocuments/classification-schemes/threats-classification-scheme

  74. 74.

    The IUCN Red List of Threatened Species Version 2006 (ICUN, 2006); http://www.iucnredlist.org

  75. 75.

    Salafsky, N. et al. A standard lexicon for biodiversity conservation: unified classifications of threats and actions. Conserv. Biol. 22, 897–911 (2008).

  76. 76.

    Maxwell, S. L., Fuller, R. A., Brooks, T. M. & Watson, J. E. M. Biodiversity: the ravages of guns, nets and bulldozers. Nature 536, 143–145 (2016).

Download references

Acknowledgements

We thank N. Upham, I. Quintero, R. Freckleton, D. Wake, J. Tonini, the GWU systematics group, and the VertLife group for discussions and comments on the manuscript. We are grateful to M. Duong for help with the figure design. We acknowledge support from NSF DEB-1441737, DEB-1558568 and NSF DBI-1262600 to W.J. and DEB-1441719 and DBI-0905765 to R.A.P.

Author information

Affiliations

  1. Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA

    • Walter Jetz
  2. Division of Biology, Imperial College London, Ascot, UK

    • Walter Jetz
  3. Department of Biological Sciences, The George Washington University, Washington DC, USA

    • R. Alexander Pyron

Authors

  1. Search for Walter Jetz in:

  2. Search for R. Alexander Pyron in:

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Walter Jetz or R. Alexander Pyron.

Supplementary information

  1. Supplementary Information

    Supplementary Materials and Methods; Supplementary Results and Analyses; Supplementary References; Supplementary Figures S1–S12.

  2. Life Sciences Reporting Summary

  3. Supplementary Table S1

    Evolutionary distinctness and threat status data for species in analysis

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/s41559-018-0515-5