Restricted access
Articles
Articles
Investing in evolutionary history: implementing a phylogenetic approach for mammal conservation
Published:27 September 2011https://doi.org/10.1098/rstb.2011.0109
Abstract
Under the impact of human activity, global extinction rates have risen a thousand times higher than shown in the fossil record. The resources available for conservation are insufficient to prevent the loss of much of the world's threatened biodiversity during this crisis. Conservation planners have been forced to prioritize their protective activities, in the context of great uncertainty. This has become known as ‘the agony of choice’. A range of methods have been proposed for prioritizing species for conservation attention; one of the most strongly supported is prioritizing those species that maximize phylogenetic distinctiveness (PD). We evaluate how a composite measure of extinction risk and phylogenetic isolation (EDGE) has been used to prioritize species according to their degree of unique evolutionary history (evolutionary distinctiveness, ED) weighted by conservation urgency (global endangerment, GE). We review PD-based approaches and provide an updated list of EDGE mammals using the 2010 IUCN Red List. We evaluate how robust this method is to changes in phylogenetic uncertainty, knowledge of taxonomy and extinction risk, and examine how mammalian species that rank highly in EDGE score are representative of the collective from which they are drawn.
Footnotes
References
- 1
Butchart S. H. M., 2010 Global biodiversity decline continues. Science 328, 1164–1168.doi:10.1126/science.1187512 (doi:10.1126/science.1187512). Crossref, PubMed, ISI, Google Scholar - 2
Collen B., Loh J., Holbrook S., McRae L., Amin R.& Baillie J. E. M. . 2009 Monitoring change in vertebrate abundance: the Living Planet Index. Conserv. Biol. 23, 317–327.doi:10.1111/j.1523-1739.2008.01117.x (doi:10.1111/j.1523-1739.2008.01117.x). Crossref, PubMed, ISI, Google Scholar - 3
Crozier R. H. . 1997 Preserving the information content of species: genetic diversity, phylogeny, and conservation worth. Annu. Rev. Ecol. Syst. 28, 243–268.doi:10.1146/annurev.ecolsys.28.1.243 (doi:10.1146/annurev.ecolsys.28.1.243). Crossref, Google Scholar - 4
Faith D. P. . 1992 Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10.doi:10.1016/0006-3207(92)91201-3 (doi:10.1016/0006-3207(92)91201-3). Crossref, ISI, Google Scholar - 5
Vane-Wright R. I., Humphries C. J.& Williams P. H. . 1991 What to protect—systematics and the agony of choice. Biol. Conserv. 55, 235–254.doi:10.1016/0006-3207(91)90030-D (doi:10.1016/0006-3207(91)90030-D). Crossref, ISI, Google Scholar - 6
Witting L.& Loeschcke V. . 1995 The optimization of biodiversity conservation. Biol. Conserv. 71, 205–207.doi:10.1016/0006-3207(94)00041-N (doi:10.1016/0006-3207(94)00041-N). Crossref, ISI, Google Scholar - 7
Faith D. P. . 2002 Quantifying biodiversity: a phylogenetic perspective. Conserv. Biol. 16, 248–252.doi:10.1046/j.1523-1739.2002.00503.x (doi:10.1046/j.1523-1739.2002.00503.x). Crossref, ISI, Google Scholar - 8
Cadotte M. W., Cardinale B. J.& Oakley T. H. . 2008 Evolutionary history and the effect of biodiversity on plant productivity. Proc. Natl Acad. Sci. USA 105, 17 012–17 017.doi:10.1073/pnas.0805962105 (doi:10.1073/pnas.0805962105). Crossref, ISI, Google Scholar - 9
Cadotte M. W., Cavender-Bares J., Tilman D.& Oakley T. H. . 2009 Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS ONE 4, e5695.doi:10.1371/journal.pone.0005695 (doi:10.1371/journal.pone.0005695). Crossref, PubMed, ISI, Google Scholar - 10
Redding D. W., DeWolff C. V.& Mooers A. O. . 2010 Evolutionary distinctiveness, threat status and ecological oddity in primates. Conserv. Biol. 24, 1052–1058.doi:10.1111/j.1523-1739.2010.01532.x (doi:10.1111/j.1523-1739.2010.01532.x). Crossref, PubMed, ISI, Google Scholar - 11
Magnuson-Ford K., Ingram R., Redding D. W.& Mooers A. Ø. . 2009 Rockfish (Sebastes) that are evolutionarily isolated are also large, morphologically distinctive and vulnerable to overfishing. Biol. Conserv. 142, 1787–1796.doi:10.1016/j.biocon.2009.03.020 (doi:10.1016/j.biocon.2009.03.020). Crossref, ISI, Google Scholar - 12
Cadotte M. W.& Davies T. J. . 2010 Rarest of the rare: advances in combining evolutionary distinctiveness and scarcity to inform conservation at biogeographical scales. Divers. Distrib. 16, 376–385.doi:10.1111/j.1472-4642.2010.00650.x (doi:10.1111/j.1472-4642.2010.00650.x). Crossref, ISI, Google Scholar - 13
Mace G. M., Gittleman J. L.& Purvis A. . 2003 Preserving the Tree of Life. Science 300, 1707–1709.doi:10.1126/science.1085510 (doi:10.1126/science.1085510). Crossref, PubMed, ISI, Google Scholar - 14
Mace G. M.& Purvis A. . 2008 Evolutionary biology and practical conservation: bridging a widening gap. Mol. Ecol. 17, 9–19.doi:10.1111/j.1365-294X.2007.03455.x (doi:10.1111/j.1365-294X.2007.03455.x). Crossref, PubMed, ISI, Google Scholar - 15
Bininda-Emonds O. R. P. . 2004 The evolution of supertrees. Trends Ecol. Evol. 19, 315–322.doi:10.1016/j.tree.2004.03.015 (doi:10.1016/j.tree.2004.03.015). Crossref, PubMed, ISI, Google Scholar - 16
Baillie J. E. M., Griffiths J., Turvey S. T., Loh J.& Collen B. . 2010 Evolution lost: status and trends of the world's vertebrates. UK: Zoological Society of London. Google Scholar - 17
Bennett P. M.& Owens I. P. F. . 1997 Variation in extinction risk among birds: chance or evolutionary predisposition. Proc. R. Soc. Lond. B 264, 401–408.doi:10.1098/rspb.1997.0057 (doi:10.1098/rspb.1997.0057). Link, ISI, Google Scholar - 18
Purvis A., Agapow P.-M., Gittleman J. L.& Mace G. M. . 2000 Nonrandom extinction and the loss of evolutionary history. Science 288, 328–330.doi:10.1126/science.288.5464.328 (doi:10.1126/science.288.5464.328). Crossref, PubMed, ISI, Google Scholar - 19
Vamosi J. C.& Wilson J. R. U. . 2008 Nonrandom extinction leads to elevated loss of angiosperm evolutionary history. Ecol. Lett. 11, 1047–1053.doi:10.1111/j.1461-0248.2008.01215.x (doi:10.1111/j.1461-0248.2008.01215.x). Crossref, PubMed, ISI, Google Scholar - 20
Russell G. J., Brooks T. M., McKinney M. M.& Anderson C. G. . 1998 Present and future taxonomic selectivity in bird and mammal extinctions. Conserv. Biol. 12, 1365–1376.doi:10.1111/j.1523-1739.1998.96332.x (doi:10.1111/j.1523-1739.1998.96332.x). Google Scholar - 21
Mooers A. Ø, Goring S. J., Turvey S. T.& Kuhn T. S. . 2009 Holocene extinctions and the loss of feature diversity. Holocene extinctions (ed.& Turvey S. T. ), pp. 263–277. Oxford, UK: Oxford University Press. Crossref, Google Scholar - 22
Turvey S. T. . 2009 Holocene Extinctions. Oxford, UK: Oxford University Press. Crossref, Google Scholar - 23
Rodrigues A. S. L.& Gaston K. J. . 2002 Rarity and conservation planning across geopolitical units. Conserv. Biol. 16, 674–682.doi:10.1046/j.1523-1739.2002.00455.x (doi:10.1046/j.1523-1739.2002.00455.x). Crossref, ISI, Google Scholar - 24
Rodrigues A. S. L., 2011 Complete, accurate, mammalian phylogenies aid conservation planning, but not much. Phil. Trans. R. Soc. B 366, 2652–2660.doi:10.1098/rstb.2011.0104 (doi:10.1098/rstb.2011.0104). Link, ISI, Google Scholar - 25
Devictor V., Mouillot D., Meynard C., Jiguet F., Thuiller W.& Mouquet N. . 2010 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. PubMed, ISI, Google Scholar - 26
Forest F., 2007 Preserving the evolutionary potential of floras in biodiversity hotspots. Nature 445, 757–760.doi:10.1038/nature05587 (doi:10.1038/nature05587). Crossref, PubMed, ISI, Google Scholar - 27
Myers N., Mittermeier R. A., Mittermeier C. G., de Fonseca G. A. B.& Kent J. . 2000 Biodiversity hotspots for conservation priorities. Nature 403, 853–858.doi:10.1038/35002501 (doi:10.1038/35002501). Crossref, PubMed, ISI, Google Scholar - 28
Isaac N. J. B., Turvey S. T., Collen B., Waterman C.& Baillie J. E. M. . 2007 Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLoS ONE 2, e296.doi:10.1371/journal.pone.0000296 (doi:10.1371/journal.pone.0000296). Crossref, PubMed, ISI, Google Scholar - 29
Pavoine S., Ollier S.& Dufour A. B. . 2005 Is the originality of a species measurable? Ecol. Lett. 8, 579–586.doi:10.1111/j.1461-0248.2005.00752.x (doi:10.1111/j.1461-0248.2005.00752.x). Crossref, ISI, Google Scholar - 30
Redding D. W. . 2003 Incorporating genetic distinctness and reserve occupancy into a conservation prioritisation approach. Masters Thesis, University of East Anglia, Norwich. Google Scholar - 31
Redding D. W.& Mooers A. O. . 2006 Incorporating evolutionary measures into conservation prioritization. Conserv. Biol. 20, 1670–1678.doi:10.1111/j.1523-1739.2006.00555.x (doi:10.1111/j.1523-1739.2006.00555.x). Crossref, PubMed, ISI, Google Scholar - 32
Haake C.-J., Kashiwada A.& Su F. E. . 2008 The Shapley value of phylogenetic trees. J. Math. Biol. 56, 479–497.doi:10.1007/s00285-007-0126-2 (doi:10.1007/s00285-007-0126-2). Crossref, PubMed, ISI, Google Scholar - 33
Redding D. W., Hartmann K., Mimoto A., Bokal D., DeVos M.& Mooers A. Ø. . 2008 Evolutionarily distinctive species often capture more phylogenetic diversity than expected. J. Theor. Biol. 51, 606–615.doi:10.1016/j.jtbi.2007.12.006 (doi:10.1016/j.jtbi.2007.12.006). Crossref, ISI, Google Scholar - 34
Weitzman M. L. . 1993 What to preserve—an application of diversity theory to crane conservation. Q. J. Econ. 108, 157–183.doi:10.2307/2118499 (doi:10.2307/2118499). Crossref, ISI, Google Scholar - 35
Avise J. C. . 2005 Phylogenetic units and currencies above and below the species level. Phylogeny and conservation (eds, Purvis A., Gittleman J. L.& Brooks T. ), pp. 76–101. Cambridge, UK: Cambridge University Press. Crossref, Google Scholar - 36
Faith D. P. . 2008 Threatened species and the potential loss of phylogenetic diversity: conservation scenarios based on estimated extinction probabilities and phylogenetic risk analysis. Conserv. Biol. 22, 1461–1470.doi:10.1111/j.1523-1739.2008.01068.x (doi:10.1111/j.1523-1739.2008.01068.x). Crossref, PubMed, ISI, Google Scholar - 37
Witting L., Tomiuk J.& Loeschcke V. . 2000 Modelling the optimal conservation of interacting species. Ecol. Model. 125, 123–143.doi:10.1016/S0304-3800(99)00177-5 (doi:10.1016/S0304-3800(99)00177-5). Crossref, ISI, Google Scholar - 38
Steel M., Mimoto A.& Mooers A. Ø. . 2007 Hedging our bets: the expected contribution of species to future phylogenetic diversity. Evol. Bioinform. 3, 237–244. Crossref, PubMed, ISI, Google Scholar - 39
IUCN. 2001 IUCN Red List categories and criteria version 3.1. Gland, Switzerland: IUCN. Google Scholar
- 40
Mace G. M., Collar N. J., Gaston K. J., Hilton-Taylor C., Akcakaya H. R., Leader-Williams N., Milner-Gulland E. J.& Stuart S. N. . 2008 Quantification of extinction risk: IUCN's system for classifying threatened species. Conserv. Biol. 22, 1424–1442.doi:10.1111/j.1523-1739.2008.01044.x (doi:10.1111/j.1523-1739.2008.01044.x). Crossref, PubMed, ISI, Google Scholar - 41
Purvis A., Cardillo M., Grenyer R.& Collen B. . 2005 Correlates of extinction risk: phylogeny, biology, threat and scale. Phylogeny and conservation (eds, Purvis A., Brooks T. M.& Gittleman J. L. ), pp. 295–316. Cambridge, UK: Cambridge University Press. Crossref, Google Scholar - 42
Butchart S. H. M., Stattersfield A. J., Baillie J. E. M., Bennun L. A., Stuart S. N., Akçakaya H. R., Hilton-Taylor C.& Mace G. M. . 2005 Using Red List Indices to measure progress towards the 2010 target and beyond. Phil. Trans. R. Soc. B 360, 255–268.doi:10.1098/rstb.2004.1583 (doi:10.1098/rstb.2004.1583). Link, ISI, Google Scholar - 43
Mooers A. Ø., Faith D. P.& Maddison W. P. . 2008 Converting endangered species categories to probabilities of extinction for phylogenetic conservation prioritization. PLoS ONE 3, e3700.doi:10.1371/journal.pone.0003700 (doi:10.1371/journal.pone.0003700). Crossref, PubMed, ISI, Google Scholar - 44
Davies T. J., 2008 Phylogenetic trees and the future of mammalian biodiversity. Proc. Natl Acad. Sci. USA 105, 11 556–11 563.doi:10.1073/pnas.0801917105 (doi:10.1073/pnas.0801917105). Crossref, ISI, Google Scholar - 45
Agnarsson I., Kuntner M.& May-Collado L. . 2010 Dogs, cats, and kin: a molecular species-level phylogeny of Carnivora. Mol. Phylogenet. Evol. 54, 726–745.doi:10.1016/j.ympev.2009.10.033 (doi:10.1016/j.ympev.2009.10.033). Crossref, PubMed, ISI, Google Scholar - 46
Butchart S. H. M.& Bird J. P. . 2010 Data Deficient birds on the IUCN Red List: what don't we know and why does it matter. Biol. Conserv. 143, 239–247.doi:10.1016/j.biocon.2009.10.008 (doi:10.1016/j.biocon.2009.10.008). Crossref, ISI, Google Scholar - 47
Collen B., Ram M., Dewhurst N., Clausnitzer V., Kalkman V. J., Cumberlidge N.& Baillie J. E. M. . 2009 Broadening the coverage of biodiversity assessments. Wildlife in a changing world—an analysis of the 2008 IUCN Red List of threatened species (eds, Vié J.-C., Hilton-Taylor C.& Stuart S. N. ), pp. 67–76. Gland, Switzerland: IUCN. Google Scholar - 48
Schipper J., 2008 The status of the world's land and marine mammals: diversity, threat, and knowledge. Science 322, 225–230.doi:10.1126/science.1165115 (doi:10.1126/science.1165115). Crossref, PubMed, ISI, Google Scholar - 49
- 50
Hoffmann M., 2010 The impact and shortfall of conservation on the status of the world's vertebrates. Science 330, 1503–1509.doi:10.1126/science.1194442 (doi:10.1126/science.1194442). Crossref, PubMed, ISI, Google Scholar - 51
Bininda-Emonds O. R. P., 2007 The delayed rise of present-day mammals. Nature 446, 507–512.doi:10.1038/nature05634 (doi:10.1038/nature05634). Crossref, PubMed, ISI, Google Scholar - 52
Bininda-Emonds O. R. P., 2008 The delayed rise of present-day mammals: corrigendum. Nature 456, 274.doi:10.1038/nature07347 (doi:10.1038/nature07347). Crossref, ISI, Google Scholar - 53
Fritz S. A., Bininda-Emonds O. R. P.& Purvis A. . 2009 Geographical variation in predictors of mammalian extinction risk: big is bad, but only in the tropics. Ecol. Lett. 12, 538–549.doi:10.1111/j.1461-0248.2009.01307.x (doi:10.1111/j.1461-0248.2009.01307.x). Crossref, PubMed, ISI, Google Scholar - 54
Wilson D. E.& Reeder D. M. . 2005 Mammal species of the world: a taxonomic and geographic reference, 3rd edn. Baltimore, MD: Johns Hopkins University Press. Crossref, Google Scholar - 55
Wilson D. E.& Reeder D. M. . 1993 Mammal species of the world: a taxonomic and geographic reference, 2nd edn. Washington, DC: Smithsonian Institution Press. Google Scholar - 56
Agapow P.-M., Bininda-Emonds O. R. P., Crandall K. A., Gittleman J. L., Mace G. M., Marshall J. C.& Purvis A. . 2004 The impact of species concept on biodiversity studies. Q. Rev. Biol. 79, 161–179.doi:10.1086/383542 (doi:10.1086/383542). Crossref, PubMed, ISI, Google Scholar - 57
Isaac N. J. B., Mallet J.& Mace G. M. . 2004 Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol. Evol. 19, 464–469.doi:10.1016/j.tree.2004.06.004 (doi:10.1016/j.tree.2004.06.004). Crossref, PubMed, ISI, Google Scholar - 58
Isaac N. J. B.& Purvis A. . 2004 The ‘species problem’ and testing macroevolutionary hypotheses. Divers. Distrib. 10, 275–281.doi:10.1111/j.1366-9516.2004.00092.x (doi:10.1111/j.1366-9516.2004.00092.x). Crossref, ISI, Google Scholar - 59
Kuhn T. S., Mooers A. O.& Thomas G. H. . 2011 A simple polytomy resolver for dated phylogenies. Methods Ecol. Evol. 2, 1–10. (early online edition.) (doi:10.1111/j.2041-210X.11.00103.x). Crossref, ISI, Google Scholar - 60
Drummond A. J.& Rambaut A. . 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214.doi:10.1186/1471-2148-7-214 (doi:10.1186/1471-2148-7-214). Crossref, PubMed, ISI, Google Scholar - 61
Rambaut A.& Drummond A. J. . 2009 Tracer v1.5: an MCMC trace analysis tool. http://beast.bio.ed.ac.uk/. (accessed 1 December 2009). Google Scholar - 62
Jones K. E., 2009 PanTHERIA: a species-level database of life history, ecology and geography of extant and recently extinct mammals. Ecology 90, 2648.doi:10.1890/08-1494.1 (doi:10.1890/08-1494.1). Crossref, Google Scholar - 63
Benjamini Y.& Hochberg Y. . 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300. Crossref, Google Scholar - 64
Benjamini Y.& Yekutieli D. . 2001 The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165–1188.doi:10.1214/aos/1013699998 (doi:10.1214/aos/1013699998). Crossref, ISI, Google Scholar - 65
R Development Core Team. 2010 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See http://www.R-project.org. Google Scholar
- 66
Sitas N., Baillie J. E. M.& Isaac N. J. B. . 2009 What are we saving? Developing a standardized approach for conservation action. Anim. Conserv. 12, 231–237.doi:10.1111/j.1469-1795.2009.00244.x (doi:10.1111/j.1469-1795.2009.00244.x). Crossref, ISI, Google Scholar - 67
Bielby J., Mace G. M., Bininda-Emonds O. R. P., Cardillo M., Gittleman J. L., Jones K. E., Orme C. D. L.& Purvis A. . 2007 The fast–slow continuum in mammalian life history: an empirical reevaluation. Am. Nat. 169, 748–757.doi:10.1086/516847 (doi:10.1086/516847). Crossref, PubMed, ISI, Google Scholar - 68
Sato J. J., Yasuda S. P.& Hosoda T. . 2009 Genetic diversity of the Japanese marten (Martes melampus) and its implications for the conservation unit. Zool. Sci. 26, 457–466.doi:10.2108/zsj.26.457 (doi:10.2108/zsj.26.457). Crossref, PubMed, ISI, Google Scholar - 69
Bell N. E.& Hyvönen J. . 2010 Phylogeny of the moss clade Polytrichopsida (BRYOPHYTA): generic-level structure and incongruent gene trees. Mol. Phylogenet. Evol. 55, 381–398.doi:10.1016/j.ympev.2010.02.004 (doi:10.1016/j.ympev.2010.02.004). Crossref, PubMed, ISI, Google Scholar - 70
IUCN. 2011 Amphibian Ark Conservation Planning. http://www.amphibianark.org/about-us/aark-activities/planning-workshops/. Google Scholar
- 71
Joseph L. N., Maloney R. F.& Possingham H. P. . 2009 Optimal allocation of resources among threatened species: a project prioritization protocol. Conserv. Biol. 23, 328–338.doi:10.1111/j.1523-1739.2008.01124.x (doi:10.1111/j.1523-1739.2008.01124.x). Crossref, PubMed, ISI, Google Scholar - 72
Brandley M. C., Wang Y., Guo X., Nieto Montes de Oca A., Fería Ortíz M., Hikida T., Ota H.& Rankin D. J. . 2010 Bermuda as an evolutionary life raft for an ancient lineage of endangered lizards. PLoS ONE 5, e11375.doi:10.1371/journal.pone.0011375 (doi:10.1371/journal.pone.0011375). Crossref, PubMed, ISI, Google Scholar - 73
Baillie J. E. M., 2008 Towards monitoring global biodiversity. Conserv. Lett. 1, 18–26.doi:10.1111/j.1755-263X.2008.00009.x (doi:10.1111/j.1755-263X.2008.00009.x). Crossref, ISI, Google Scholar - 74
Collen B.& Baillie J. E. M. . 2010 The barometer of life: sampling. Science 329, 140.doi:10.1126/science.329.5988.140-a (doi:10.1126/science.329.5988.140-a). Crossref, PubMed, ISI, Google Scholar - 75
Stuart S. N., Wilson E. O., McNeely J. A., Mittermeier R. A.& Rodriguez J. P. . 2010 The barometer of life. Science 328, 117.doi:10.1126/science.1188606 (doi:10.1126/science.1188606). Crossref, ISI, Google Scholar
