In an era of accelerated biodiversity loss and limited conservation resources, systematic prioritization of species and places is essential. In terrestrial vertebrates, evolutionary distinctness has been used to identify species and locations that embody the greatest share of evolutionary history. We estimate evolutionary distinctness for a large marine vertebrate radiation on a dated taxon-complete tree for all 1,192 chondrichthyan fishes (sharks, rays and chimaeras) by augmenting a new 610-species molecular phylogeny using taxonomic constraints. Chondrichthyans are by far the most evolutionarily distinct of all major radiations of jawed vertebrates—the average species embodies 26 million years of unique evolutionary history. With this metric, we identify 21 countries with the highest richness, endemism and evolutionary distinctness of threatened species as targets for conservation prioritization. On average, threatened chondrichthyans are more evolutionarily distinct—further motivating improved conservation, fisheries management and trade regulation to avoid significant pruning of the chondrichthyan tree of life.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Additional information

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


  1. 1.

    Wilson, K. A., McBride, M. F., Bode, M. & Possingham, H. P. Prioritizing global conservation efforts. Nature 440, 337–340 (2006).

  2. 2.

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

  3. 3.

    Waldron, A. et al. Targeting global conservation funding to limit immediate biodiversity declines. Proc. Natl. Acad. Sci. USA 110, 1–5 (2013).

  4. 4.

    Andelman, S. J. & Fagan, W. F. Umbrellas and flagships: efficient conservation surrogates or expensive mistakes? Proc. Natl. Acad. Sci. USA 97, 5954–5959 (2000).

  5. 5.

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

  6. 6.

    Faith, D. P. in The Routledge Handbook of Philosophy of Biodiversity (eds Garson, J., Plutynski, A. & Sarkar, S.) 69-85 (Routledge, New York, NY, 2017).

  7. 7.

    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).

  8. 8.

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

  9. 9.

    Stuart, S. N., Wilson, E. O., McNeely, J. A., Mittermeier, R. A. & Rodríguez, J. P. The barometer of life. Science 328, 177 (2010).

  10. 10.

    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).

  11. 11.

    Isaac, N. J. B., Redding, D. W., Meredith, H. M. & Safi, K. Phylogenetically-informed priorities for amphibian conservation. PLoS. ONE 7, 1–8 (2012).

  12. 12.

    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 (Part A), 23–31 (2016).

  13. 13.

    Heupel, M. R., Knip, D. M., Simpfendorfer, C. A. & Dulvy, N. K. Sizing up the ecological role of sharks as predators. Mar. Ecol. Prog. Ser. 495, 291–298 (2014).

  14. 14.

    Hussey, N. E. et al. Expanded trophic complexity among large sharks. Food Webs 4, 1–7 (2015).

  15. 15.

    Burkholder, D. A., Heithaus, M. R., Fourqurean, J. W., Wirsing, A. & Dill, L. M. Patterns of top-down control in a seagrass ecosystem: Could a roving apex predator induce a behaviour-mediated trophic cascade? J. Anim. Ecol. 82, 1192–1202 (2013).

  16. 16.

    Ruppert, J. L. W., Travers, M. J., Smith, L. L., Fortin, M. J. & Meekan, M. G. Caught in the middle: combined impacts of shark removal and coral loss on the fish communities of coral reefs. PLoS. ONE 8, 1–9 (2013).

  17. 17.

    Mull, C. G., Yopak, K. E. & Dulvy, N. K. Does more maternal investment mean a larger brain? Evolutionary relationships between reproductive mode and brain size in chondrichthyans. Mar. Freshw. Res. 62, 567–575 (2011).

  18. 18.

    Dulvy, N. K. & Reynolds, J. D. Evolutionary transitions among egg−laying, live−bearing and maternal inputs in sharks and rays. Proc. R. Soc. B Biol. Sci. 264, 1309–1315 (1997).

  19. 19.

    Davidson, L. N. K., Krawchuk, M. A. & Dulvy, N. K. Why have global shark and ray landings declined: Improved management or overfishing? Fish Fish 17, 438–458 (2016).

  20. 20.

    Dulvy, N. K. et al. Extinction risk and conservation of the world’s sharks and rays. eLife 3, e00590 (2014).

  21. 21.

    Redding, D. W. Incorporating Genetic Distinctness and Reserve Occupancy into a Cconservation Prioritisation Approach. MSc Thesis, Univ. East Anglia (2003).

  22. 22.

    Kuhn, T. S., Mooers, A. & Thomas, G. H. A simple polytomy resolver for dated phylogenies. Methods Ecol. Evol. 2, 427–436 (2011).

  23. 23.

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

  24. 24.

    McClenachan, L., Cooper, A. B., Carpenter, K. E. & Dulvy, N. K. Extinction risk and bottlenecks in the conservation of charismatic marine species. Conserv. Lett. 5, 73–80 (2012).

  25. 25.

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

  26. 26.

    Mace, G. M. et al. Quantification of extinction risk: IUCN’s system for classifying threatened species. Conserv. Biol. 22, 1424–1442 (2008).

  27. 27.

    IUCN The IUCN Red List of Threatened Species Version 2014.1 (IUCN, 2014).

  28. 28.

    Verde Arregoitia, L. D., Blomberg, S. P. & Fisher, D. O. Phylogenetic correlates of extinction risk in mammals: species in older lineages are not at greater risk. Proc. Biol. Sci. 280, 20131092 (2013).

  29. 29.

    Field, I. C., Meekan, M. G., Buckworth, R. C. & Bradshaw, C. J. A. Susceptibility of sharks, rays and chimaeras to global extinction. Adv. Mar. Biol. 56, 275–363 (2009).

  30. 30.

    Dulvy, N. K. et al. Challeneges and priorities in shark and ray conservation. Curr. Biol. 27, R565–R572 (2017).

  31. 31.

    Lucifora, L. O., García, V. B. & Worm, B. Global diversity hotspots and conservation priorities for sharks. PLoS. ONE 6, e19356 (2011).

  32. 32.

    Trebilco, R. et al. Mapping species richness and human impact drivers to inform global pelagic conservation prioritisation. Biol. Conserv. 144, 1758–1766 (2011).

  33. 33.

    Davidson, L. N. K. & Dulvy, N. K. Global marine protected areas to prevent extinctions. Nat. Ecol. Evol. 1, 0040 (2017).

  34. 34.

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

  35. 35.

    Lennon, J. J., Koleff, P., Greenwood, J. J. D. & Gaston, K. J. Contribution of rarity and commonness to patterns of species richness. Ecol. Lett. 7, 81–87 (2004).

  36. 36.

    Tittensor, D. P. et al. Global patterns and predictors of marine biodiversity across taxa. Nature 466, 1098–1101 (2010).

  37. 37.

    Orme, C. D. L. et al. Global hotspots of species richness are not congruent with endemism or threat. Nature 436, 1016–1019 (2005).

  38. 38.

    Clarke, S. C. et al. Global estimates of shark catches using trade records from commercial markets. Ecol. Lett. 9, 1115–1126 (2006).

  39. 39.

    McClenachan, L., Cooper, A. B. & Dulvy, N. K. Rethinking trade-driven extinction risk in marine and terrestrial megafauna. Curr. Biol. 26, 1–7 (2016).

  40. 40.

    Curtis, T. H. et al. Seasonal distribution and historic trends in abundance of white sharks, Carcharodon carcharias, in the western North Atlantic Ocean. PLoS. ONE 9, e99240 (2014).

  41. 41.

    Lowe, C. G. et al. in Global Perspectives on the Biology and Life History of the White Shark (ed. Domeier, M.) 169–186 (CRC Press, Boca Raton, FL 2012).

  42. 42.

    Simpfendorfer, C. A. & Dulvy, N. K. Bright spots of sustainable shark fishing. Curr. Biol. 27, R97–R98 (2017).

  43. 43.

    Giles, J., Riginos, C., Naylor, G., Dharmadi & Ovenden, J. Genetic and phenotypic diversity in the wedgefish Rhynchobatus australiae, a threatened ray of high value in the shark fin trade. Mar. Ecol. Prog. Ser. 548, 165–180 (2016).

  44. 44.

    Devitt, K. R., Adams, V. M. & Kyne, P. M. Australia’s protected area network fails to adequately protect the world’s most threatened marine fishes. Glob. Ecol. Conserv. 3, 401–411 (2015).

  45. 45.

    Dulvy, N. K. et al. Ghosts of the coast: global extinction risk and conservation of sawfishes. Aquat. Conserv. Mar. Freshw. Ecosyst. 26, 134–153 (2016).

  46. 46.

    Moore, A. Guitarfishes: the next sawfishes? Extinction vulnerabilites and an urgent call for conservaion action.Endanger. Species Res. 34, 75–88 (2017).

  47. 47.

    Davies, T. J. & Buckley, L. B. Phylogenetic diversity as a window into the evolutionary and biogeographic histories of present-day richness gradients for mammals. Philos. Trans. R. Soc. B Biol. Sci. 366, 2414–2425 (2011).

  48. 48.

    Fernandes, P. et al. Fisheries conservation reveals regional divergence in Europe’s marine fish risk.Nat. Ecol. Evol. 1, 0170 (2017).

  49. 49.

    Peterson, C. D. et al. Preliminary recovery of coastal sharks in the south-east United States.Fish. Fish. 18, 845–859 (2017).

  50. 50.

    White, W. T. & Kyne, P. M. The status of chondrichthyan conservation in the Indo-Australasian region. J. Fish. Biol. 76, 2090–2117 (2010).

  51. 51.

    Naylor, G. J. P. et al. in The Biology of Sharks and Their Relatives (eds Carrier, J. C., Musick, J. A. & Heithaus, M. R.) 31–56 (CRC Press, Boca Raton, FL, 2012).

  52. 52.

    Naylor, G. J. P. et al. A DNA sequence-based approach to the identification of shark and ray species and its implications for globa elasmobranch diversity and parasitology. Bull. Am. Mus. Nat. Hist. 367, 1–262 (2012).

  53. 53.

    Naylor, G. J. P., Ryburn, J. A., Fedrigo, O. & López, J. A. in Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids, and Chimaeras (eds Hamlett, W. C. & Jamieson, B. G.) 1–25 (CRC Press, Boca Raton, FL, 2005).

  54. 54.

    White, W. T. & Last, P. R. A review of the taxonomy of chondrichthyan fishes: a modern perspective. J. Fish. Biol. 80, 901–917 (2012).

  55. 55.

    Last, P. R. et al. Rays of the World (CSIRO Publishing, Clayton South, 2016).

  56. 56.

    Last, P. R. et al. in Rays of the World, Supplementary Information 1–10 (CSIRO Publishing, Clayton South, 2016).

  57. 57.

    Last, P. R., Weigmann, S. & Yang, L. in Rays of the World, Supplementary Information 11–34 (CSIRO Publishing, Clayton South, 2016).

  58. 58.

    Weigmann, S. Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity. J. Fish. Biol. 88, 837–1037 (2016).

  59. 59.

    Weigmann, S. Reply to Borsa (2017): comment on ‘Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity by Weigmann (2016)’. J. Fish. Biol. 88, 837–1037 (2017).

  60. 60.

    Ebert, D. A., Fowler, S. L. & Compagno, L. J. V. Sharks of the World: A Fully Illustrated Guide (Wild Nature Press, Plymouth, 2013).

  61. 61.

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

  62. 62.

    Katoh, K., Kuma, K. I., Toh, H. & Miyata, T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511–518 (2005).

  63. 63.

    Katoh, K. & Toh, H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 9, 286–298 (2008).

  64. 64.

    Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059–3066 (2002).

  65. 65.

    Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772–772 (2012).

  66. 66.

    Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003).

  67. 67.

    Yang, Z. Computational Molecular Evolution (Oxford Univ. Press, Oxford, 2006).

  68. 68.

    Inoue, J. G. et al. Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective. Mol. Biol. Evol. 27, 2576–2586 (2010).

  69. 69.

    Aschliman, N. C. et al. Body plan convergence in the evolution of skates and rays (Chondrichthyes: Batoidea). Mol. Phylogenet. Evol. 63, 28–42 (2012).

  70. 70.

    Aberer, A. J., Krompass, D. & Stamatakis, A. Pruning rogue taxa improves phylogenetic accuracy: an efficient algorithm and webservice. Syst. Biol. 62, 162–166 (2013).

  71. 71.

    Parham, J. F. et al. Best practices for justifying fossil calibrations. Syst. Biol. 61, 346–359 (2012).

  72. 72.

    Benton, M. J. et al. Constraints on the timescale of animal evolutionary history. Palaeontol. Electron. 18, 1–107 (2015).

  73. 73.

    Lund, R. & Grogan, E. D. Relationships of the Chimaeriformes and the basal radiation of the Chondrichthyes. Rev. Fish. Biol. Fish. 7, 65–123 (1997).

  74. 74.

    Claeson, K. M., Underwood, C. J. & Ward, D. J. Tingitanius tenuimandibulus, a new platyrhinid batoid from the Turonian (Cretaceous) of Morocco and the cretaceous radiation of the Platyrhinidae. J. Vertebr. Paleontol. 33, 1019–1036 (2013).

  75. 75.

    Carvalho, M. R. De & Maisey, J. G. Phylogenetic relationships of the Late Jurassic shark Protospinax WOODWARD 1919 (Chondrichthyes: Elasmobranchii). Syst. Paleoecol. 7, 9–46 (1996).

  76. 76.

    Ho, S. Y. W. & Phillips, M. J. Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst. Biol. 58, 367–380 (2009).

  77. 77.

    Smith, S. A. & O’Meara, B. C. TreePL: divergence time estimation using penalized likelihood for large phylogenies. Bioinformatics 28, 2689–2690 (2012).

  78. 78.

    Venkatesh, B. et al. Elephant shark genome provides unique insights into gnathostome evolution. Nature 505, 174–179 (2014).

  79. 79.

    Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).

  80. 80.

    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).

  81. 81.

    Hartmann, K. The equivalence of two phylogenetic biodiversity measures: the Shapley value and fair proportion index. J. Math. Biol. 67, 1163–1170 (2013).

  82. 82.

    Fuchs, M. & Jin, E. Y. Equality of Shapley value and fair proportion index in phylogenetic trees. J. Math. Biol. 71, 1133–1147 (2015).

  83. 83.

    Shapley, L. S. A value for n-person games. Ann. Math. Stud. 28, 307–318 (1953).

  84. 84.

    Haake, C.-J., Kashiwada, A. & Su, F. E. The Shapley value of phylogenetic trees. J. Math. Biol. 56, 479–497 (2008).

  85. 85.

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

  86. 86.

    Mooers, A., Gascuel, O., Stadler, T., Li, H. & Steel, M. Branch lengths on birth-death trees and the expected loss of phylogenetic diversity. Syst. Biol. 61, 195–203 (2012).

  87. 87.

    Redding, D. W., Mazel, F. & Mooers, A. Measuring evolutionary isolation for conservation. PLoS. ONE 9, 1–15 (2014).

  88. 88.

    Orme, D. et al. caper: comparative analysis of phylogenetics and evolution in R (2012).

  89. 89.

    Rondinini, C., Wilson, K. A., Boitani, L., Grantham, H. & Possingham, H. P. Tradeoffs of different types of species occurrence data for use in systematic conservation planning. Ecol. Lett. 9, 1136–1145 (2006).

  90. 90.

    Rodrigues, A. S. L. Improving coarse species distribution data for conservation planning in biodiversity-rich, data-poor, regions: no easy shortcuts. Anim. Conserv. 14, 108–110 (2011).

  91. 91.

    Jenness Enterprises Repeating shapes for ArcGIS (Jenness Enterprises, 2012).

  92. 92.

    Hoffmann, M. et al. The impact of conservation on the status of the world’s vertebrates. Science 330, 1503–1509 (2010).

  93. 93.

    Pompa, S., Ehrlich, P. R. & Ceballos, G. Global distribution and conservation of marine mammals. Proc. Natl. Acad. Sci. USA 108, 13600–13605 (2011).

  94. 94.

    Davidson, A. D. et al. Drivers and hotspots of extinction risk in marine mammals. Proc. Natl. Acad. Sci. USA 109, 3395–3400 (2012).

  95. 95.

    R Core Team R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2013).

  96. 96.

    Wickham, H. The split–apply–combine strategy for data. J. Stat. Softw. 40, 1–29 (2011).

  97. 97.

    Pebesma, E. J. & Bivand, R. S. Classes and method for spatial data in R. R. News 5, 9–13 (2005).

  98. 98.

    ESRI ArcGIS (ESRI, 2011).

  99. 99.

    VLIZ World EEZ v7 (VLIZ, 2014).

Download references


We are grateful to A. J. Aberer for useful discussion of rogue taxon exclusion, D. Ebert and W. White for taxonomic guidance, G. J. P. Naylor, X. Vélez-Zauzo, A. Godknecht, M. Gollock, H. Koldewey and M. D’Angelo for research support, and B. Corrie and M. Siegert for computing access. We thank all IUCN Shark Specialist Group members and all additional experts who have contributed data and their expertise to IUCN Red List assessments. This work was carried out at the Interdisciplinary Research in Mathematics and Computer Sciences Centre, Simon Fraser University (http://www.irmacs.sfu.ca), the Swiss Shark Foundation computing cluster and Compute Canada’s Westgrid computing network. This study was funded by Save Our Seas Foundation, Rufford Foundation, Zoological Society London, Natural Science and Engineering Research Council Discovery and Accelerator Awards, and Canada Research Chairs Program. Shark and ray silhouettes in Figs. 1, 2 and 4 were created by C.G.M from images by R. Aidan Martin; all silhouettes in Fig. 3 were created by M. Dando.

Author information

Author notes

  1. R. William Stein and Christopher G. Mull contributed equally to this work.


  1. Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada

    • R. William Stein
    • , Christopher G. Mull
    • , Lindsay N. K. Davidson
    • , Gordon J. Smith
    • , Nicholas K. Dulvy
    •  & Arne O. Mooers
  2. Scimitar Scientific, Whitehorse, Yukon, Canada

    • Tyler S. Kuhn
  3. Biology Department, St Ambrose University, Davenport, IA, USA

    • Neil C. Aschliman
  4. BC Centre for Excellence in HIV/AIDS, University of British Columbia, Vancouver, British Columbia, Canada

    • Jeffrey B. Joy
  5. Department of Medicine, University of British Columbia, Vancouver, British Columbia, Canada

    • Jeffrey B. Joy


  1. Search for R. William Stein in:

  2. Search for Christopher G. Mull in:

  3. Search for Tyler S. Kuhn in:

  4. Search for Neil C. Aschliman in:

  5. Search for Lindsay N. K. Davidson in:

  6. Search for Jeffrey B. Joy in:

  7. Search for Gordon J. Smith in:

  8. Search for Nicholas K. Dulvy in:

  9. Search for Arne O. Mooers in:


N.K.D. and A.O.M. conceived and led the project, R.W.S., C.G.M., J.B.J., T.S.K., N.C.A., L.N.K.D. and A.O.M. designed the project. N.C.A., R.W.S., C.G.M., J.B.J., G.J.S. and L.N.K.D. acquired or provided data. R.W.S., T.S.K., J.B.J. and L.N.K.D. contributed essential code and analyses. R.W.S., C.G.M., L.N.K.D., N.K.D. and A.O.M. drafted and revised the paper. R.W.S. designed and led the phylogenetic work, C.G.M. supported the phylogenetic work and led the subsequent statistical analyses, and L.N.K.D. led the spatial analyses.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Christopher G. Mull or Nicholas K. Dulvy or Arne O. Mooers.

Supplementary information

  1. Supplementary Information

    Supplementary results and tables

  2. Life Sciences Reporting Summary

  3. Supplementary table 1

    Master taxonomy dataset

  4. Supplementary table 2

    Accession dataset

  5. Supplementary table 3

    Fossil calibration dataset

  6. Supplementary table 4

    Mixed clade and tree modification dataset

  7. Supplementary table 5

    Vertebrate comparison dataset

  8. Supplementary table 6

    Recently described species dataset

  9. Supplementary code 1

    Species addition R script

  10. Supplementary code 2

    Polytomy resolver R script

  11. Supplementary code 3

    XML creator R script

About this article

Publication history






Further reading