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Spatial conservation prioritization of biodiversity spanning the evolutionary continuum

Nature Ecology & Evolution volume 1, Article number: 0151 (2017) Cite this article

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Abstract

Accounting for evolutionary relationships between and within species is important for biodiversity conservation planning, but is rarely considered in practice. Here we introduce a novel framework to identify priority conservation areas accounting for phylogenetic and intraspecific diversity, integrating concepts from phylogeny, phylogeography, spatial statistics and spatial conservation prioritization. The framework allows planners to incorporate and combine different levels of evolutionary diversity and can be applied to any taxonomic group and to any region in the world. We illustrate our approach using amphibian and reptile species occurring in a biodiversity hotspot region, the Iberian Peninsula. We found that explicitly incorporating phylogenetic and intraspecific diversity in systematic conservation planning provides advantages in terms of maximizing overall biodiversity representation while enhancing its persistence and evolutionary potential. Our results emphasize the need to account for the evolutionary continuum in order to efficiently implement biodiversity conservation planning decisions.

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Figure 1: Methodological workflow and illustration of features’ weights.
Figure 2: Spatial patterns of diversity for the amphibian and reptile species of the Iberian Peninsula.
Figure 3: Comparison of Zonation solutions (areas included in the highest 17% rank) between the Sp scenario and the alternatives (Br, SpLin and BrLin) for both amphibians and reptiles.
Figure 4: Relative and target efficiencies.

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References

  1. Watson, J. E. M., Dudley, N., Segan, D. B. & Hockings, M. The performance and potential of protected areas. Nature 515, 67–73 (2014).

    Article  CAS  Google Scholar 

  2. Myers, N., Mittermeler, R. A., Mittermeler, C. G., da Fonseca, G. A. B. & Kent, J. Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000).

    Article  CAS  Google Scholar 

  3. Eken, G. et al. Key biodiversity areas as site conservation targets. Bioscience 54, 1110–1118 (2004).

    Article  Google Scholar 

  4. Margules, C. & Sarkar, S. Systematic Conservation Planning (Cambridge Univ. Press, 2007).

    Google Scholar 

  5. Moilanen, A ., Possingham, H. P. & Wilson, K. A. in Spatial Conservation Prioritization—Quantitative Methods and Computational Tools (eds Moilanen, A., Wilson, K. A. & Possingham, H. P. ) (Oxford Univ. Press, 2009).

    Google Scholar 

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

    Article  Google Scholar 

  7. Crandall, K. A., Bininda-Emonds, O. R. P., Mace, G. M. & Wayne, R. K. Considering evolutionary processes in conservation biology. Trends Ecol. Evol. 15, 290–295 (2000).

    Article  CAS  Google Scholar 

  8. Moritz, C. Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst. Biol. 51, 238–254 (2002).

    Article  Google Scholar 

  9. Vane-Wright, R. I., Humphries, C. J. & Williams, P. H. What to protect? Systematics and the agony of choice. Biol. Conserv. 2, 235–254 (1991).

    Article  Google Scholar 

  10. Srivastava, D. S., Cadotte, M. W., MacDonald, A. A. M., Marushia, R. G. & Mirotchnick, N. Phylogenetic diversity and the functioning of ecosystems. Ecol. Lett. 15, 637–648 (2012).

    Article  Google Scholar 

  11. Pollock, L. J. et al. Phylogenetic diversity meets conservation policy: small areas are key to preserving eucalypt lineages. Phil. Trans. R. Soc. Lond. B Biol. Sci. 370, 20140007 (2015).

    Article  Google Scholar 

  12. Asmyhr, M. G., Linke, S., Hose, G. & Nipperess, D. A. Systematic conservation planning for groundwater ecosystems using phylogenetic diversity. PLoS ONE 9, e115132 (2014).

    Article  Google Scholar 

  13. Forest, F. et al. Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445, 757–760 (2007).

    Article  CAS  Google Scholar 

  14. Veron, S., Davies, T. J., Cadotte, M. W., Clergeau, P. & Pavoine, S. Predicting loss of evolutionary history: where are we? Biol. Rev. 92, 271–291 (2015).

    Article  Google Scholar 

  15. Diniz-Filho, J. A. F., Loyola, R. D., Raia, P., Mooers, A. O. & Bini, L. M. Darwinian shortfalls in biodiversity conservation. Trends Ecol. Evol. 28, 689–695 (2013).

    Article  Google Scholar 

  16. Rodrigues, A. S. L ., Brooks, T. M. & Gaston, K. J. in Phylogeny and Conservation (eds Purvis, A., Gittleman, J. & Brooks, T. ) 101–119 (Cambridge Univ. Press, 2005).

    Book  Google Scholar 

  17. Devictor, V. et al. Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol. Lett. 13, 1030–1040 (2010).

    PubMed  Google Scholar 

  18. Tucker, C. M. & Cadotte, M. W. Unifying measures of biodiversity: understanding when richness and phylogenetic diversity should be congruent. Divers. Distrib. 19, 845–854 (2013).

    Article  Google Scholar 

  19. Morlon, H. et al. Spatial patterns of phylogenetic diversity. Ecol. Lett. 14, 141–149 (2011).

    Article  Google Scholar 

  20. Reed, D. H. & Frankham, R. Correlation between fitness and genetic diversity. Conserv. Biol. 17, 230–237 (2003).

    Article  Google Scholar 

  21. Frankham, R. & Ralls, K. Inbreeding leads to extinction. Nature 392, 441–442 (1998).

    Article  CAS  Google Scholar 

  22. Sgro, C. M., Lowe, A. J. & Hoffmann, A. A. Building evolutionary resilience for conserving biodiversity under climate change. Evol. Appl. 4, 326–337 (2011).

    Article  Google Scholar 

  23. Tarroso, P., Velo-Antón, G. & Carvalho, S. B. phylin: an r package for phylogeographic interpolation. Mol. Ecol. Resour 15, 349–357 (2015).

    Article  Google Scholar 

  24. Rosauer, D. F., Catullo, R. A., VanDerWal, J., Moussalli, A. & Moritz, C. Lineage range estimation method reveals fine-scale endemism linked to Pleistocene stability in Australian rainforest herpetofauna. PLoS ONE 10, e0126274 (2015).

    Article  Google Scholar 

  25. Funk, W. C., McKay, J. K., Hohenlohe, P. A. & Allendorf, F. W. Harnessing genomics for delineating conservation units. Trends Ecol. Evol. 27, 489–496 (2012).

    Article  Google Scholar 

  26. Hewitt, G. M. Some genetic consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58, 247–276 (1996).

    Article  Google Scholar 

  27. Carnaval, A. C. et al. Prediction of phylogeographic endemism in an environmentally complex biome. Proc. R. Soc. Lond. B Biol. Sci. 281, 20141461 (2014).

    Article  Google Scholar 

  28. Thomassen, H. A. et al. Mapping evolutionary process: a multi-taxa approach to conservation prioritization. Evol. Appl. 4, 397–413 (2011).

    Article  Google Scholar 

  29. Vasconcelos, R., Brito, J. C., Carvalho, S. B., Carranza, S. & Harris, D. J. Identifying priority areas for island endemics using genetic versus specific diversity—the case of terrestrial reptiles of the Cape Verde Islands. Biol. Conserv. 153, 276–286 (2012).

    Article  Google Scholar 

  30. Rissler, L. J., Hijmans, R. J., Graham, C. H., Moritz. C. & Wake, D. B. Phylogeographic lineages and species comparisons in conservation analyses: a case study of california herpetofauna. Am. Nat. 167, 655–666 (2006).

    Article  Google Scholar 

  31. Pope, L. C., Liggins, L., Keyse, J., Carvalho, S. B. & Riginos, C. Not the time or the place: the missing spatio-temporal link in publicly available genetic data. Mol. Ecol. 24, 3802–3809 (2015).

    Article  Google Scholar 

  32. Brooks, T. M. et al. Why and how might genetic and phylogenetic diversity be reflected in the identification of key biodiversity areas? Phil. Trans. R. Soc. Lond. B Biol. Sci. 370, 3802–3809 (2015).

    Article  Google Scholar 

  33. Rosauer, D., Laffan, S. W., Crisp, M. D., Donnellan, S. C. & Cook, L. G. Phylogenetic endemism: a new approach for identifying geographical concentrations of evolutionary history. Mol. Ecol. 18, 406–407 (2009).

    Article  Google Scholar 

  34. 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  Google Scholar 

  35. Bennett, J. R. et al. Balancing phylogenetic diversity and species numbers in conversation prioritization, using a case study of threatened species in New Zealand. Biol. Conserv. 174, 47–54 (2014).

    Article  Google Scholar 

  36. Gómez, A. & Lunt, D. H. in Phylogeography of Southern European Refugia (eds Weiss, S. & Ferrand, N. ) 155–188 (Springer, 2006).

    Google Scholar 

  37. Strecker, A. L., Olden, J. D., Whittier, J. B. & Paukert, C. P. Defining conservation priorities for freshwater fishes according to taxonomic, functional, and phylogenetic diversity. Ecol. Appl. 21, 3002–3013 (2011).

    Article  Google Scholar 

  38. Rodrigues, A. S. L. et al. Complete, accurate, mammalian phylogenies aid conservation planning, but not much. Phil. Trans. R. Soc. Lond. B Biol. Sci. 366, 2652–2660 (2011).

    Article  Google Scholar 

  39. Ponce-Reyes, R., Clegg, S. M., Carvalho, S. B., McDonald-Madden, E. & Possingham, H. P. Geographic surrogates of genetic variation for selecting island populations for conservation. Divers. Distrib. 20, 640–651 (2014).

    Article  Google Scholar 

  40. Vernesi, C. et al. Where's the conservation in conservation genetics? Conserv. Biol. 22, 802–804 (2008).

    Article  Google Scholar 

  41. Mace, G. M. & Purvis, A. Evolutionary biology and practical conservation: bridging a widening gap. Mol. Ecol. 17, 9–19 (2008).

    Article  Google Scholar 

  42. Beger, M. et al. Evolving coral reef conservation with genetic information. Bull. Mar. Sci. 90, 159–185 (2014).

    Article  Google Scholar 

  43. Angeloni, F., Wagemaker, N., Vergeer, P. & Ouborg, J. Genomic toolboxes for conservation biologists. Evol. Appl. 5, 130–143 (2012).

    Article  CAS  Google Scholar 

  44. Fitzpatrick, M. C. & Keller, S. R. Ecological genomics meets community-level modelling of biodiversity: mapping the genomic landscape of current and future environmental adaptation. Ecol. Lett. 18, 1–16 (2015).

    Article  Google Scholar 

  45. Loureiro, A., Ferrand de Almeida, N., Carretero, M. A. & Paulo, O. S. Atlas dos Anfíbios e Répteis de Portugal (Instituto da Conservação da Natureza e da Biodiversidade, 2008).

  46. Pleguezuelos, J. M ., Márquez, R. & Lizana, M. Atlas y Libro Rojo de los Anfíbios y Reptiles de España (Dirección General de Conservación de la Naturaleza, Asociación Herpetologica Española, 2002).

    Google Scholar 

  47. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  49. R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014).

  50. Zhang, J., Pei, N. & Mi, X. phylotools: phylogenetic tools for eco-phylogenetics (2015); https://cran.r-project.org/web/packages/phylotools/index.html

  51. Reid, N. M. & Carstens, B. C. Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evol. Biol. 12, 196 (2012).

    Article  Google Scholar 

  52. Moilanen, A. et al. Zonation—spatial conservation planning methods and software. Version 4. User Manual. 290 (C-BIG Conservation Biology Informatics Group, Univ. Helsinki, 2014).

  53. Rodrigues, A. S. L. & Gaston, K. J. Maximising phylogenetic diversity in the selection of networks of conservation areas. Biol. Conserv. 105, 103–111 (2002).

    Article  Google Scholar 

  54. Moilanen, A. et al. Prioritizing multiple-use landscapes for conservation: methods for large multi-species planning problems. Proc. R. Soc. Lond. B Biol. Sci. 272, 1885–1891 (2005).

    Article  Google Scholar 

  55. Ball, I. R., Possingham, H. P. & Watts, M. E. in Spatial Conservation Prioritization - Quantitative Methods and Computational Tools (eds Moilanen, A., Wilson, K. A. & Possingham, H. P. ) 185–195 (Oxford Univ. Press, 2009).

    Google Scholar 

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Acknowledgements

This work was developed under the project PTDC/BIABIC/118624/2010, funded by Fundação para a Ciência e Tecnologia (FCT) through the North of Portugal Regional Operational Programme 2007/2013 (ON.2O Novo Norte), the National Strategic Reference Framework (NSRF), and the European Regional Development Fund (ERDF); and through project PTDC/BIA-BIC/3545/2014, supported by Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF). P.T. and S.B.C. were funded by FCT postdoctoral grants (SFRH/BPD/93473/2013 and SFRH/BPD/74423/2010, respectively) and G.V.-A. was supported by an IF contract (IF/01425/2014), attributed by FCT. S.C. was funded by project CGL2015-70390-P (MINECO/FEDER). H.P.P. was supported by the Australian Research Council. We thank all the colleagues who kindly provided samples and molecular data: A. Perera, A. Miraldo, A. Kaliontzopoulou, B. Carvalho, C. Rato, D. Guicking, F. F. Martínez, H. Gonçalves, I. Martínez-Solano, J. Harris, M. Fonseca, M. Carretero, N. Sillero, R. Godinho, R. Cunha, U. Fritz and X. Santos.

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Authors and Affiliations

  1. CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, R. Padre Armando Quintas, Vairão, 4485-661, Portugal.

    Silvia B. Carvalho, Guillermo Velo-Antón, Pedro Tarroso, Ana Paula Portela & Mafalda Barata

  2. The School of Biological Sciences, University of Queensland, St Lucia, Queensland 4072, Australia.

    Silvia B. Carvalho & Hugh P. Possingham

  3. Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, E-08003, Spain.

    Salvador Carranza

  4. Research School of Biology and Centre for Biodiversity Analysis, The Australian National University, Acton,, ACT 6201, Australia.

    Craig Moritz

  5. Conservation Science, The Nature Conservancy, West End, Queensland 4101, Australia.

    Hugh P. Possingham

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  1. Silvia B. Carvalho
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Contributions

S.B.C., S.C., C.M. and H.P.P. designed the study. S.B.C., P.T. and A.P.P. compiled the data. M.B., G.V.-A. and S.C. collected field samples. M.B. carried out the laboratory work. G.V.A. and S.C. performed the molecular analysis. P.T. and S.B.C. performed the lineage’s occurrence analysis. S.B.C. and A.P.P. performed the spatial prioritization analysis. S.B.C. led the writing, to which all authors contributed.

Corresponding author

Correspondence to Silvia B. Carvalho.

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The authors declare no competing financial interests.

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Supplementary Information

Details on study area; Supplementary Methods; Supplementary References; Supplementary Tables 1–6; Supplementary phylogenetic trees. (PDF 2509 kb)

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Carvalho, S., Velo-Antón, G., Tarroso, P. et al. Spatial conservation prioritization of biodiversity spanning the evolutionary continuum. Nat Ecol Evol 1, 0151 (2017). https://doi.org/10.1038/s41559-017-0151

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