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

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.

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Fig. 1: Lineage-through-time plots of 100 time trees sampled from the Bayesian posterior distribution.
Fig. 2: Variation in net diversification rates of the three amphibian clades.
Fig. 3: Phylogeny of all extant amphibian species and their variation in ED.
Fig. 4: Biogeographic variation in amphibian phylogenetic structure as characterized by the probability density of ED values.
Fig. 5: ED of the top 100 most evolutionarily distinct amphibian species (median ED: >54 Myr) and their 2016 IUCN Red List threat status and clade affinity.
Fig. 6: Variation in ED by threat status categorization and main threat.

References

  1. 1.

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

    CAS  Article  PubMed  Google Scholar 

  2. 2.

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

    CAS  Article  PubMed  Google Scholar 

  3. 3.

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

    Article  PubMed  Google Scholar 

  4. 4.

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

    CAS  Article  PubMed  Google Scholar 

  5. 5.

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

    CAS  Article  PubMed  Google Scholar 

  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).

    CAS  Article  PubMed  Google Scholar 

  7. 7.

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

    CAS  Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  9. 9.

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

    Article  Google Scholar 

  10. 10.

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

    CAS  Article  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

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

    Article  PubMed  Google Scholar 

  13. 13.

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

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  17. 17.

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

    CAS  Article  PubMed  Google Scholar 

  18. 18.

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

    CAS  Article  PubMed  Google Scholar 

  19. 19.

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

    CAS  Article  PubMed  Google Scholar 

  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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  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).

    CAS  Article  PubMed  Google Scholar 

  22. 22.

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

    CAS  Article  PubMed  Google Scholar 

  23. 23.

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

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

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

    Article  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

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

    Article  PubMed  Google Scholar 

  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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  PubMed  Google Scholar 

  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).

    CAS  Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

  41. 41.

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

    Article  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

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

    CAS  Article  PubMed  Google Scholar 

  44. 44.

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

    Article  PubMed  Google Scholar 

  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).

    CAS  Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  49. 49.

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

    CAS  Article  PubMed  Google Scholar 

  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).

    CAS  Article  PubMed  Google Scholar 

  51. 51.

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

    Article  PubMed  Google Scholar 

  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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

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

    Article  Google Scholar 

  54. 54.

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

    Article  PubMed  PubMed Central  Google Scholar 

  55. 55.

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  57. 57.

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

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  65. 65.

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

    CAS  Article  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  70. 70.

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

    CAS  Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    CAS  Article  PubMed  Google Scholar 

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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.

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Correspondence to Walter Jetz or R. Alexander Pyron.

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

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Evolutionary distinctness and threat status data for species in analysis

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Jetz, W., Pyron, R.A. The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat Ecol Evol 2, 850–858 (2018). https://doi.org/10.1038/s41559-018-0515-5

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