Building evolutionary resilience for conserving biodiversity under climate change

Abstract

Evolution occurs rapidly and is an ongoing process in our environments. Evolutionary principles need to be built into conservation efforts, particularly given the stressful conditions organisms are increasingly likely to experience because of climate change and ongoing habitat fragmentation. The concept of evolutionary resilience is a way of emphasizing evolutionary processes in conservation and landscape planning. From an evolutionary perspective, landscapes need to allow in situ selection and capture high levels of genetic variation essential for responding to the direct and indirect effects of climate change. We summarize ideas that need to be considered in planning for evolutionary resilience and suggest how they might be incorporated into policy and management to ensure that resilience is maintained in the face of environmental degradation.

Literature cited Bailey, J., J. Schweitzer, F. Ubeda, J. Koricheva, C. LeRoy, M. Madritch, B. Rehill et al. 2009. From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization. Philosophical Transactions of the Royal Society B 362:1607–1616. Balanya, J., L. Serra, G. W. Gilchrist, R. B. Huey, M. Pascual, F. Mestres, and E. Sole. 2003. Evolutionary pace of chromosomal polymorphism in colonizing populations of Drosophila subobscura: an evolutionary time series. Evolution 57:1837–1845. Beaumont, M., and D. Balding. 2004. Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology 13:969–980. Berkelmans, R., and M. J. H. van Oppen. 2006. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget’ of hope for coral reefs in an era of climate change. Proceedings of the Royal Society B 273:2305–2312. Bonin, A., F. Nicole, F. Pompanon, C. Miaud, and P. Taberlet. 2007. Population adaptive index: a new method to help measure intraspecific geneytic diversity and prioritize populations for conservation. Conservation Biology 21:697–708. Bradshaw, W. E., and C. M. Holzapfel. 2008. Genetic response to rapid climate change: it’s seasonal timing that matters. Molecular Ecology 17:157–166. Broadhurst, L., A. Young, P. Thrall, and B. Murray. 2006. Sourcing seed for Acacia acinacea, a key revegetation species in south eastern Australia. Conservation Genetics 7:749–763. Broadhurst, L. M., A. Lowe, D. J. Coates, S. A. Cunningham, M. McDonald, P. A. Vesk, and C. Yates. 2008. Seed supply for broadscale restoration: maximising evolutionary potential. Evolutionary Applications 1:587–597. Burdon, R., and P. Wilcox. 2007. Population management:potential impacts of advances in genomics. New Forests 34:187–206. Burger, R., and M. Lynch. 1995. Evolution and extinction in a changing environment – a quantitative-genetic analysis. Evolution 49:151–163. Butcher, P., M. McDonald, and J. Bell. 2009. Congruence between environmental parameters, morphology and genetic structure in Australia’s most widely distributed eucalypt, Eucalyptus camaldulensis. Tree Genomics & Genomes 5:189–210. Callaham, R. 1964. Provenance research: investigation of genetic diversity associated with geography. Unasylva 18:40–50. Charmantier, A., R. McCleery, L. Cole, C. Perrins, L. Kruuk, and B. Sheldon. 2009. Adaptive phenotpyic plasticity in response to climate change in a wild bird population. Science 320:800–803. Chevin, L.-M., R. Lande, and G. M. Mace. 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biology 8:e1000357. Cheviron, Z., and R. Brumfield. 2009. Migration-selection balance and local adaptation of mitochondrial haplotypes in rufoucollared sparrows (Zonotrichia capensis) along an elevational gradient. Evolution 63:1593–1605. Cowling, R. M., and R. L. Pressey. 2001. Rapid plant diversification: planning for an evolutionary future. Proceedings of the National Academy of Sciences USA 98:5452–5457. Crandall, K. 2009. A multifacted approach to species conservation. Animal Conservation 12:105–106. Crozier, R. H. 1997. Preserving the information content of species: genetic diversity, phylogeny, and conservation worth. Annual Review of Ecology and Systematics 28:243–268. Crozier, L. 2004. Field transplants reveal summer constraints on a butterfly range expansion. Oecologia 141:148–157. Davis, E. B., M. S. Koo, C. Conroy, J. L. Patton, and C. Moritz. 2008. The California Hotspots Project: identifying regions of rapid diversification of mammals. Molecular Ecology 17:120–138. Deutsch, C. A., J. J. Tewksbury, R. B. Huey, K. S. Sheldon, C. K. Ghalambour, D. C. Haak, and P. R. Martin. 2008. Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences USA 105:6668–6672. Dorman, M., Y. Sapir, and S. Volis. 2009. Local adaptation in four Iris species tsted in a common garden experiment. Biological Journal of the Linnean Society 98:267–277. Dunlop, M., and P. R. Brown. 2008. Implications of climate change for Australia’s National Reserve System: A Preliminary Assessment. A Report to the Department of Climate Change, February 2008. Department of Climate Change, Canberra, Australia. Edmands, S. 2007. Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology 16:463–475. Etterson, J. R., and R. G. Shaw. 2001. Constraint to adaptive evolution in response to global warming. Science 294:151–154. Fortuna, M., R. Albaladejo, L. Fernandez, A. Aparicio, and J. Bascompte. 2009. Networks of spatial genetic variation across species. Proceedings of the National Academy of Sciences USA 10:19044–19049. Frankham, R. 2008. Genetic adaptation to captivity in species conservation programs. Molecular Ecology 17:325–333. Frankham, R., J. D. Ballou, and D. A. Briscoe. 2002. Introduction to Conservation Genetics. Cambridge University Press, Cambridge. Garnier-Gere, P. H., and P. K. Ades. 2001. Environmental surrogates for predicting and conserving adaptive genetic variability in tree species. Conservation Biology 15:1632–1644. Gebremedhin, B., G. Ficetola, S. Naderi, H.-R. Rezaei, C. Maudet, D. Rioux, G. Luikart et al. 2009. Frontiers in developing conservation units: from neutral markers to adaptive genetic variation. Animal Conservation 12:107–109. Gibson, A., E. P. Bachelard, and K. T. Hubick. 1995. Relationship between climate and provenance variation in Eucalyptus camaldulensis Dehnh. Australian Journal of Plant Physiology 22:453–460. Grueber, C. E., and I. G. Jamieson. 2008. Quantifying and managing the loss of genetic variation in a free-ranging population of takahe through the use of pedigrees. Conservation Genetics 9:645–651. Gunderson, L. 2000. Ecological resilience – in theory and application. Annual Review of Ecology and Systematics 31:425–439. Hadfield, J. D., A. J. Wilson, D. Garant, B. C. Sheldon, and L. E. B. Kruuk. 2010. The misuse of BLUP in ecology and evolution. American Naturalist 175:116–125. Hannah, L. 2010. A global conservation system for climate change adaptation. Conservation Biology 24:70–77. Hannah, L., G. Midgley, G. Hughes, and B. Bomhard. 2005. The view from the cape. Extinction risk, protected areas, and climate change. BioScience 55:231–242. Hannah, L., G. Midgley, S. Andelman, M. Araujo, G. Hughes, E. Martinez-Meyer, R. Pearson et al. 2007. Protected area needs in a changing climate. Frontiers in Ecology and the Environment 5:131–138. Hellmann, J., and M. Pineda-Krch. 2007. Constraints and reinforcement on adaptation under climate change: selection of genetically correlated traits. Biological Conservation 137:599–609. Hendry, A. P., L. G. Lohmann, E. Conti, J. Cracraft, K. A. Crandall, D. P. Faith, C. Hauser et al. 2010. Evolutionary biology in biodiversity science, conservation, and policy: a call to action. Evolution 64:1517–1528. Hereford, J. 2009. A quantiative survey of local adaptation and fitness trade-offs. The American Naturalist 173:579–588. Hoegh-Guldberg, O., L. Hughes, S. McIntyre, D. B. Lindenmayer, C. Parmesan, H. P. Possingham, and C. D. Thomas. 2008. Assisted colonization and rapid climate change. Science 321:345–346. Hoffmann, A. A., and A. R. Weeks. 2007. Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 129:133–147. Hoffmann, A. A., and Y. Willi. 2008. Detecting genetic responses to environmental change. Nature Reviews Genetics 9:1–12. Holmes, G. D., E. A. James, and A. A. Hoffmann. 2008. Limitations to reproductive output and genetic rescue in populations of the rare shrub Grevillea repens (Proteaceae). Annals of Botany 102:1031–1041. Hunter, M. L. 2007. Climate change and moving species: furthering the debate on assisted colonization. Conservation Biology 21:1356–1358. Jamieson, I., G. Wallis, and J. Briske. 2006. Inbreeding and endangered species management: is New Zealand out of step with teh rest of the world? Conservation Biology 20:38–47. Johansson, M., C. Primmer, and J. Merila. 2007. Does habitat fragmentation reduce fitness and adaptability? A case study of the common frog (Rana temporaria). Molecular Ecology 16:2693–2700. Jones, T. A., and T. A. Monaco. 2009. A role for assisted evolution in designing native plant materials for domesticated landscapes. Frontiers in Ecology and the Environment 7:541–547. Joost, S., A. Bonin, M. W. Bruford, L. Despres, C. Conord, G. Erhadrt, and P. Taberlet. 2007. A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Molecular Ecology 16:3955–3969. Kearney, M., W. P. Porter, C. Williams, S. Ritchie, and A. A. Hoffmann. 2009. Integrating biophysical models and evolutionary theory to predict climatic impacts on species’ ranges: the dengue mosquito Aedes aegypti in Australia. Functional Ecology 23:528–538. Keller, M., J. Kollman, and P. Edwards. 2000. Genetic introgression from distant provenances reduces fitness in local weed populations. Journal of Applied Ecology 37:647–659. Kellermann, V. M., B. van Heerwaarden, A. A. Hoffmann, and C. M. Sgro. 2006. Very low additive genetic variance and evolutionary potential in multiple populations of two rainforest Drosophila species. Evolution 60:1104–1108. Kellermann, V., B. van Heerwaarden, C. Sgro, and A. Hoffmann. 2009. Fundamental evolutionary limits in ecological traits drive Drosophila species distributions. Science 325:1244–1246. Klemme, I., and I. Hanski. 2009. Heritability of and strong single gene (Pgi) effects on life history traits in the Glanville fritillary butterfly. Journal of Evolutionary Biology 22:1944–1953. Kozak, K., C. Graham, and J. Wiens. 2008. Integrating GIS-based environmental data into evolutionary biology. Trends in Ecology & Evolution 23:141–148. Kruuk, L., J. Slate, and A. Wilson. 2008. New answers for old questions: the evolutionary quantitative genetics of wild animal populations. Annual Review of Ecology, Evolution and Systematics 39:525–548. Lipow, S. R., K. Vance-Borland, J. B. St Clair, J. Henderson, and C. McCain. 2004. Gap analysis of conserved genetic resources for forest trees. Conservation Biology 18:412–423. Lipow, S., K. Vance-Borland, J. St Clair, J. Henderson, and C. McCain. 2007. In situ gene conservation of six conifers in western Washington and Oregon. Western Journal of Applied Forestry 22:176–187. Lopez, S., F. Rousset, F. Shaw, R. Shaw, and O. Ronce. 2009. Joint effects of inbreeding and local adaptation on the evolution of genetic load after fragmentation. Conservation Biology 23:1618–1627. Lynch, M., and R. Lande. 1993. Evolution and extinction in response to environmental change. In P. M. Kareiva, J. G. Kingsolver, and R. B. Huey, eds. Biotic Interactions and Global Change, pp. 234–250. Sinauer Associates Inc., Sunderland, Massachusetts. Mace, G. M., and A. Purvis. 2008. Evolutionary biology and practical conservation: bridging a widening gap. Molecular Ecology 17:9–19. Mackey, B. G., M. E. Soule, H. A. Nix, H. F. Recher, R. G. Lesslie, J. E. Williams, J. C. Z. Woinarski et al. 2007. Towards a scientific framework for the Wild Country project. In J. Wu, and R. J. Hobbs, eds. Key Topics and Perspectives in Landscape Ecology, pp. 192–208. Cambridge University Press, Cambridge. Mansergh, I., and D. Cheal. 2007. Protected Area Planning and Management for Eastern Australian Temperate Forests and Woodland Ecosystems. Protected Areas: Buffering Nature Against Climate Change, Sydney, Australia. WWF-Australia, Sydney. McKay, J. K., and R. G. Latta. 2002. Adaptive population divergence: markers, QTL and traits. Trends in Ecology & Evolution 17:285–291. McKay, J., C. Christian, S. Harrison, and K. Rice. 2005. “How local is local?”– a review of practical and conceptual issues in the genetics of restoration. Restoration Ecology 13:432–440. McLachlan, J. S., J. J. Hellmann, and M. W. Schwartz. 2007. A frmework for debate of assisted migration in an era of climate change. Conservation Biology 21:297–302. McRae, B. H., and P. Beier. 2007. Circuit theory predicts gene flow in plant and animal populations. Proceedings of the National Academy of Sciences USA 104:19885–19890. Menges, E. S. 2008. Restoration demography and genetics of plants: when is a translocation successful? Australian Journal of Botany 56:187–196. Miskelly, C., G. Taylor, H. Gummer, and R. Williams. 2009. Translocations of eight species of burrow-nesting seabirds (genera Pterodromoa, Pelecanoides, Pachyptila and Puffinus: Family Procellariidae). Biological Conservation 142:1965–1980. Mitrovski, P., A. Hoffmann, D. Heinze, and A. Weeks. 2008. Rapid loss of genetic variation in an endangered possum. Biology Letters 4:134–138. Moritz, C. 2002. Strategies to protect biological diversity and the evolutionary processes that sustain it. Systematic Biology 51:238–254. Moritz, C., C. Hoskin, C. H. Graham, A. Hugall, and A. Moussalli. 2009. Historical biogeography, diversity and conservation of Australia’s tropical rainforest herpetofauna. In A. Purvis, J. L. Gittleman, and T. Brooks, eds. Phylogeny and Conservation, pp. 243–267. Cambridge University Press, Cambridge. O’Brien, E., R. Mazanec, and S. Krauss. 2007. Provenance variation of ecologically important traits of forest trees: implications for restoration. Journal of Applied Ecology 44: pp. 583–595. Ozgul, A., S. Tuljapurkar, T. Benton, J. Pemberton, T. Clutton-Brock, and T. Coulson. 2009. The dynamics of phenotypic change and teh shrinking sheep of St. Kilda. Science 325:464–467. Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology Evolution and Systematics 37:637–669. Pavlacky, D., A. Goldizen, P. Prentis, J. Nicholls, and A. Lowe. 2009. A landscape genetics approach for quantifying the relative influence of historic and contemporary habitat heterogeneity on the genetic connectivity of a rainforest bird. Molecular Ecology 18:2945–2960. Pelini, S. L., J. D. K. Dzurisin, K. M. Prior, C. M. Williams, T. D. Marsico, B. J. Sinclair, and J. J. Hellmann. 2009. Translocation experiments with butterflies reveal limits to enhancement of poleward populations under climate change. Proceedings of the National Academy of Sciences USA 106:11160–11165. Pressey, R. L., M. Cabeza, M. E. Watts, R. M. Cowling, and K. A. Wilson. 2007. Conservation planning in a changing world. Trends in Ecology and Evolution 22:583–592. Ramirez-Valiente, J., Z. Lorenzo, A. Soto, F. Valladares, L. Gil, and I. Aranda. 2009. Elucidating the role of genetic drift and natural selection in cork oak differentiation regarding drought tolerance. Molecular Ecology 18:3803–3815. Reed, D. H., and R. Frankham. 2001. How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103. Reusch, T., and T. Wood. 2007. Molecular ecology of global change. Molecular Ecology 16:3973–3992. Reusch, T. B., A. Ehlers, A. Hammerli, and B. Worm. 2005. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proceedings of the National Academy of Sciences USA 102:2826–2831. Ricciardi, A., and D. Simberloff. 2009. Assisted colonization is not a viable conservation strategy. Trends in Ecology & Evolution 24:248–253. Rice, K., and N. C. Emery. 2003. Managing microevolution: restoration in the face of global change. Frontiers in Ecology and the Environment 1:469–478. Richardson, D. M., J. J. Hellmann, J. S. McLachlan, D. F. Sax, M. W. Schwartz, P. Gonzalez, E. J. Brennan et al. 2009. Multidimensional evaluation of managed relocation. Proceedings of the National Academy of Sciences USA 106:9721–9724. Root, T. L., J. T. Price, K. R. Hall, S. H. Schneider, C. Rosenzweig, and J. A. Pounds. 2003. Fingerprints of global warming on wild animals and plants. Nature 421:57–60. Rouget, M., R. M. Cowling, A. T. Lombard, A. T. Knight, and G. H. Kerley. 2006. Designing large-scale conservation corridors for pattern and process. Conservation Biology 20:549–561. Schneider, C. J., T. B. Smith, B. Larison, and C. Moritz. 1999. A test of alternative models of diversification in tropical rainforests: ecological gradient vs. rainforest refugia. Proceedings of the National Academy of Sciences USA 96:13869–13873. Soule, M. E., B. G. Mackey, H. F. Recher, J. E. Williams, J. C. Z. R. Woinarski, D. Driscol, W. C. Dennison et al. 2004. The role of connectivity in Australian conservation. Pacific Conservation Biology 10:266–279. Spielman, D., B. W. Brook, and R. Frankham. 2004. Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences USA 101:15261–15264. Storz, J. 2005. Using genome scans of DNA polymorphisms to infer adaptive population divergence. Molecular Ecology 14:671–688. Swarts, N. D., and K. W. Dixon. 2009. Terrestrial orchid conservation in the age of extinction. Annals of Botany 104:543–556. Taylor, M., and P. Figgis. 2007. Protected Areas: Buffering Nature Against Climate Change, Sydney, Australia. WWF-Australia, Sydney. Thomas, C. D., A. Cameron, R. E. Green, M. Bakkenes, L. J. Beaumont, Y. C. Collingham, B. F. N. Erasmus et al. 2004. Extinction risk from climate change. Nature 427:145–148. Thrush, S. F., J. E. Hewitt, P. K. Dayton, G. Coco, A. M. Lohrer, A. Norkko, J. Norkko et al. 2009. Forecasting the limits of resilience: integrating empirical research with theory. Proceedings of the Royal Society B-Biological Sciences 276:3209–3217. Umina, P. A., A. R. Weeks, M. R. Kearney, S. W. McKechnie, and A. A. Hoffmann. 2005. A rapid shift in a classic clinal pattern in Drosophila reflecting climate change. Science 308:691–693. Vandergast, A. G., A. J. Bohonak, S. A. Hathaway, J. Boys, and R. N. Fisher. 2008. Are hotspots of evolutionary potential adequately protected in southern California? Biological Conservation 141:1648–1664. Viveros-Viveros, H., C. Saenz-Romeroa, J. Vargas-Hernandez, J. Lopez-Upton, G. Ramirez-Valverde, and A. Santacruz-Varela. 2009. Altitudinal variation in Pinus hartwegii Lindl. I: height growth, shoot phenology and frost damage in seedlings. Forest Ecology and Management 257:836–842. Wearne, L. J., and J. W. Morgan. 2001. Recent forest encroachment into subalpine grasslands near Mount Hotham, Victoria, Australia. Arctic Antarctic and Alpine Research 33:369–377. Whitham, T. G., J. K. Bailey, J. A. Schweitzer, S. M. Shuster, R. K. Bangert, C. J. LeRoy, E. V. Lonsdorf et al. 2006. A framework for community and ecosystem genetics: from genes to ecosystems. Nature Reviews Genetics 7:510–523. Whitlock, M. 1999. Neutral additive genetic variance in a metapopulation. Genetical Research 74:215–221. Wilkinson, D. 2001. Is local provenance important in habitat creation? Journal of Applied Ecology 38:1371–1373. Willi, Y., and A. A. Hoffmann. 2008. Demographic factors and genetic variation influence population persistence under environmental change. Journal of Evolutionary Biology 22:124–133. Willi, Y., J. van Buskirk, and A. A. Hoffmann. 2006. Limits to the adaptive potential of small populations. Annual Review of Ecology, Evolution and Systematics 37:433–478. Williams, S. E., E. E. Bolitho, and S. Fox. 2003. Climate change in Australian tropical forests: an impending environmental catastrophe. Proceedings of the Royal Society, London, Series B: Biological Sciences 270:1887–1892.