Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Predicting impacts of global climate change on intraspecific genetic diversity benefits from realistic dispersal estimates

Paul E. Duckett A B and Adam J. Stow A

A Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia.

B Corresponding author. Email: paul.duckett@mq.edu.au

Australian Journal of Zoology 61(6) 454-461 http://dx.doi.org/10.1071/ZO13097
Submitted: 13 November 2013  Accepted: 13 February 2014   Published: 3 March 2014

Abstract

Global climates are rapidly changing, which for many species will require dispersal to higher altitudes and latitudes to maintain favourable conditions. Changes in distribution for less mobile species is likely to be associated with losses to genetic diversity, yet this cannot be quantified without understanding which parts of a species distribution will colonise favourable regions in the future. To address this we adopted a realistic estimate of dispersal with predicted changes in species distributions to estimate future levels of intraspecific genetic diversity. Using 740 geckos (Gehyra variegata) collected across their distribution in central and eastern inland Australia, we predict genetic loss within phylogenetically distinct units at both mtDNA and microsatellite markers between 2010 and 2070. We found that using a quantified and realistic estimate of dispersal resulted in significant declines to allelic richness (5.114 to 4.052), haplotype richness (7.215 to 4.589) and phylogenetic diversity (0.012 to 0.005) (P < 0.01). In comparison, predicted losses were substantially over- or underestimated when commonly applied dispersal scenarios were utilised. Using biologically relevant estimates of dispersal will help estimate losses of intraspecific genetic diversity following climate change impacts. This approach will provide critical information for the management of species in the near future.

Graphical Abstract Image

Additional keywords: conservation, modelling.


References

Alsos I. G. Ehrich D. Thuiller W. Eidesen P. B. Tribsch A. Schönswetter P. Lagaye C. Taberlet P. Brochmann C. 2012 Genetic consequences of climate change for northern plants. Proceedings of the Royal Society B: Biological Sciences 279 2042 –2051

Araújo, M. B., and New, M. (2007). Ensemble forecasting of species distributions. Trends in Ecology & Evolution 22, 42–47.
Ensemble forecasting of species distributions.CrossRef | open url image1

Arenas, M., Ray, N., Currat, M., and Excoffier, L. (2012). Consequences of range contractions and range shifts on molecular diversity. Molecular Biology and Evolution 29, 207–218.
Consequences of range contractions and range shifts on molecular diversity.CrossRef | 1:CAS:528:DC%2BC3MXhs1ynu77P&md5=9b2e257e8612dd99d8b39dc9f78fec7dCAS | 21778191PubMed | open url image1

Arenas, M., Francois, O., Currat, M., Ray, N., and Excoffier, L. (2013). Influence of admixture and paleolithic range contractions on current European diversity gradients. Molecular Biology and Evolution 30, 57–61.
Influence of admixture and paleolithic range contractions on current European diversity gradients.CrossRef | 1:CAS:528:DC%2BC38XhvV2gtrzP&md5=a7c2dee3440c7d1bbc899ef33e51d912CAS | 22923464PubMed | open url image1

Balint, M., Domisch, S., Engelhardt, C. H. M., Haase, P., Lehrian, S., Sauer, J., Theissinger, K., Pauls, S. U., and Nowak, C. (2011). Cryptic biodiversity loss linked to global climate change. Nature Climate Change 1, 313–318.
Cryptic biodiversity loss linked to global climate change.CrossRef | open url image1

Beier, P., and Gregory, A. J. (2012). Desperately seeking stable 50-year old landscapes with patches and long, wide corridors. PLoS Biology 10, e1001253.
Desperately seeking stable 50-year old landscapes with patches and long, wide corridors.CrossRef | 1:CAS:528:DC%2BC38XisV2mt74%3D&md5=fe52f5cc66555b3d8d21177e5f2e01a1CAS | 22303283PubMed | open url image1

Bohonak, A. J. (1999). Dispersal, gene flow, and population structure. The Quarterly Review of Biology 74, 21–45.
Dispersal, gene flow, and population structure.CrossRef | 1:STN:280:DyaK1M7otFKltw%3D%3D&md5=240a4e514aa74078bf8a2d59173108cbCAS | 10081813PubMed | open url image1

Bustard, H. R. (1968). The ecology of the Australian gecko, Gehyra variegata, in northern New South Wales. Journal of Zoology 154, 113–138.
The ecology of the Australian gecko, Gehyra variegata, in northern New South Wales.CrossRef | open url image1

Byrne, M. (2008). Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quaternary Science Reviews 27, 2576–2585.
Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography.CrossRef | open url image1

CBD (1992). International Convention on Biological Diversity. Available at: www.cbd.int

Cogger, H. G. (2000). ‘Reptiles and Amphibians of Australia.’ (Reed New Holland: Sydney.)

Costa, G., Nogueira, C., Machado, R., and Colli, G. (2010). Sampling bias and the use of ecological niche modeling in conservation planning: a field evaluation in a biodiversity hotspot. Biodiversity and Conservation 19, 883–899.
Sampling bias and the use of ecological niche modeling in conservation planning: a field evaluation in a biodiversity hotspot.CrossRef | open url image1

Crandall, K. A., Bininda-Emonds, O. R. P., Mace, G. M., and Wayne, R. K. (2000). Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution 15, 290–295.
Considering evolutionary processes in conservation biology.CrossRef | open url image1

Davis, M. B., and Shaw, R. G. (2001). Range shifts and adaptive responses to quaternary climate change. Science 292, 673–679.
Range shifts and adaptive responses to quaternary climate change.CrossRef | 1:CAS:528:DC%2BD3MXjt1elsrY%3D&md5=57804a8869fe37d7b7f9379ae358fec6CAS | 11326089PubMed | open url image1

Duckett, P. E., and Stow, A. (2010). Rapid isolation and characterisation of microsatellite loci from a widespread Australian gecko, the tree dtella, Gehyra variegata. Conservation Genetics Resources 2, 349–351.
Rapid isolation and characterisation of microsatellite loci from a widespread Australian gecko, the tree dtella, Gehyra variegata.CrossRef | open url image1

Duckett, P. E., and Stow, A. J. (2012). Levels of dispersal and tail loss in an Australian gecko (Gehyra variegata) are associated with differences in forest structure. Australian Journal of Zoology 59, 170–176.
Levels of dispersal and tail loss in an Australian gecko (Gehyra variegata) are associated with differences in forest structure.CrossRef | open url image1

Duckett, P. E., and Stow, A. J. (2013). Higher genetic diversity is associated with stable water refugia for a gecko with a wide distribution in arid Australia. Diversity & Distributions 19, 1072–1083.
Higher genetic diversity is associated with stable water refugia for a gecko with a wide distribution in arid Australia.CrossRef | open url image1

Duckett, P. E., Wilson, P. D., and Stow, A. J. (2013). Keeping up with the neighbours: using a genetic estimate of dispersal and species distribution modelling to assess the impact of climate change on an Australian arid zone gecko (Gehyra variegata). Diversity & Distributions 19, 964–976.
Keeping up with the neighbours: using a genetic estimate of dispersal and species distribution modelling to assess the impact of climate change on an Australian arid zone gecko (Gehyra variegata).CrossRef | open url image1

Engler, R., and Guisan, A. (2009). MigClim: predicting plant distribution and dispersal in a changing climate. Diversity & Distributions 15, 590–601.
MigClim: predicting plant distribution and dispersal in a changing climate.CrossRef | open url image1

Frankham, R. (1996). Relationship of genetic variation to population size in wildlife. Conservation Biology 10, 1500–1508.
Relationship of genetic variation to population size in wildlife.CrossRef | open url image1

Frankham, R., Ballou, J. D., and Briscoe, D. A. (2004). Introduction. In ‘Conservation Genetics’. 4th edn. (Cambridge University Press: Cambridge.)

Frankham, R., Ballou, J. D., Eldridge, M. D. B., Lacy, R. C., Ralls, K., Dudash, M. R., and Fenster, C. B. (2011). Predicting the probability of outbreeding depression. Conservation Biology 25, 465–475.
Predicting the probability of outbreeding depression.CrossRef | 21486369PubMed | open url image1

Franklin, J. (2010). Moving beyond static species distribution models in support of conservation biogeography. Diversity & Distributions 16, 321–330.
Moving beyond static species distribution models in support of conservation biogeography.CrossRef | open url image1

Gienapp, P., Teplitsky, C., Alho, J.S., Mills, J.A., and Merilä, J (2008). Climate change and evolution: disentangling environmental and genetic responses. Molecular Ecology 17, 167–178.
Climate change and evolution: disentangling environmental and genetic responses.CrossRef | 1:STN:280:DC%2BD1c%2Fgsl2muw%3D%3D&md5=a20133a8a0a9ad0f9080ee70f753d186CAS | 18173499PubMed | open url image1

Goudet, J. (2001). ‘FSTAT, a Program to Estimate Test Gene Diversities and Fixation Indices (Version 2.9.3)’.

Grenouillet, G., Buisson, L., Casajus, N., and Lek, S. (2011). Ensemble modelling of species distribution: the effects of geographical and environmental ranges. Ecography 34, 9–17.
Ensemble modelling of species distribution: the effects of geographical and environmental ranges.CrossRef | open url image1

Guisan, A., and Thuiller, W. (2005). Predicting species distribution: offering more than simple habitat models. Ecology Letters 8, 993–1009.
Predicting species distribution: offering more than simple habitat models.CrossRef | open url image1

Gustafson, P., Hossain, S., and Macnab, Y. C. (2006). Conservative prior distributions for variance parameters in hierarchical models. The Canadian Journal of Statistics 34, 377–390.
Conservative prior distributions for variance parameters in hierarchical models.CrossRef | open url image1

Habitats Directive of the European Union (1992). On the conservation of natural habitats and of wild fauna and flora. Council Directive 92/42/EEC. (ec.europe.eu/environment/nature/legislation/habitatsdirective)

Halverson, M. A., Skelly, D. K., and Caccone, A. (2006). Inbreeding linked to amphibian survival in the wild but not in the laboratory. The Journal of Heredity 97, 499–507.
Inbreeding linked to amphibian survival in the wild but not in the laboratory.CrossRef | 1:CAS:528:DC%2BD28Xht1OjsbvL&md5=8ddb5cb804069f66d0d3bae07b8249eeCAS | 16957048PubMed | open url image1

Heller, N. E., and Zavaleta, E. S. (2009). Biodiversity management in the face of climate change: a review of 22 years of recommendations. Biological Conservation 142, 14–32.
Biodiversity management in the face of climate change: a review of 22 years of recommendations.CrossRef | open url image1

Henle, K. (1990). Population ecology and life history of the arboreal gecko Gehyra variegata in arid Australia. Herpetological Monograph 4, 30–60.
Population ecology and life history of the arboreal gecko Gehyra variegata in arid Australia.CrossRef | open url image1

Hewitt, G. M. (1996). Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society of London 58, 247–276. open url image1

Hoehn, M., and Sarre, S. (2006). Microsatellite DNA markers for Australian geckos. Conservation Genetics 7, 795–798.
Microsatellite DNA markers for Australian geckos.CrossRef | 1:CAS:528:DC%2BD28XhtVWgtLrK&md5=aa982d4037ff17f457a8b93903834ae9CAS | open url image1

Hoffmann, A. A., and Willi, Y. (2008). Detecting genetic responses to environmental change. Nature Reviews: Genetics 9, 421–432.
Detecting genetic responses to environmental change.CrossRef | 1:CAS:528:DC%2BD1cXlvFKrtLw%3D&md5=ac13c94633da6fab0d1402d9793934acCAS | 18463665PubMed | open url image1

Hughes, L. (2003). Climate change and Australia: trends, projections and impacts. Austral Ecology 28, 423–443.
Climate change and Australia: trends, projections and impacts.CrossRef | open url image1

IPCC (2001). ‘Intergovernmental Panel on Climate Change – Third Assessments Report of Working Group I: The Science of Climate Change.’ (Cambridge University Press: Cambridge.)

IPCC (2007). Summary for Policymakers. In ‘Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change’. (Eds S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor, and H.L. Miller.) pp. 13–18. (Cambridge University Press: Cambridge.)

Johansson, M., Primmer, C. R., and Merilä, J (2007). Does habitat fragmentation reduce fitness and adaptability? A case study of the common frog (Rana temporaria). Molecular Ecology 16, 2693–2700.
Does habitat fragmentation reduce fitness and adaptability? A case study of the common frog (Rana temporaria).CrossRef | 17594440PubMed | open url image1

Kearney, M. R., Wintle, B. A., and Porter, W. P. (2010). Correlative and mechanistic models of species distribution provide congruent forecasts under climate change. Conservation Letters 3, 203–213.
Correlative and mechanistic models of species distribution provide congruent forecasts under climate change.CrossRef | open url image1

Lunt, D. I., Byrne, M., Hellmann, J. J., Mitchell, N. J., Garnett, S. T., Hayward, M. W., Martine, T. G., McDonald-Madden, E., Williams, S. E., and Zander, K. K. (2013). Using assisted colonisation to conserve biodiversity and restore ecosystem function under climate change. Biological Conservation 157, 172–177.
Using assisted colonisation to conserve biodiversity and restore ecosystem function under climate change.CrossRef | open url image1

Marmion, M., Parviainen, M., Luoto, M., Heikkinen, R. K., and Thuiller, W. (2009). Evaluation of consensus methods in predictive species distribution modelling. Diversity & Distributions 15, 59–69.
Evaluation of consensus methods in predictive species distribution modelling.CrossRef | open url image1

Moritz, C. (1994). Defining ‘Evolutionary Significant Units’. Trends in Ecology & Evolution 9, 373–375.
Defining ‘Evolutionary Significant Units’.CrossRef | 1:STN:280:DC%2BC3M7itFWhsA%3D%3D&md5=807e9b1c6637836734c00157ce889224CAS | open url image1

Moritz, C. (1999). Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130, 217–228.
Conservation units and translocations: strategies for conserving evolutionary processes.CrossRef | open url image1

Natural Resource Management Ministerial Council (2010). Australia’s Biodiversity Conservation Strategy 2010–2030. Department of the Environment. Available at: www.environment.gov.au/node/14488

Oppel, S., Meirinho, A., Ramirez, I., Gardner, B., O’Connell, A. F., Miller, P. I., and Louzao, M. (2012). Comparison of five modelling techniques to predict the spatial distribution and abundance of seabirds. Biological Conservation 156, 94–104.
Comparison of five modelling techniques to predict the spatial distribution and abundance of seabirds.CrossRef | open url image1

Pauls, S. U., Nowak, C., Bálint, M., and Pfenninger, M. (2013). The impact of global climate change on genetic diversity within populations and species. Molecular Ecology 22, 925–946.
The impact of global climate change on genetic diversity within populations and species.CrossRef | 23279006PubMed | open url image1

Peakall, R. O. D., and Smouse, P. E. (2006). Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research.CrossRef | open url image1

Phillips, B. L., Brown, G. P., Travis, J. M. L., and Shine, R. (2008). Reid’s paradox revisited: the evolution of dispersal kernels during range expansion. American Naturalist 172, 34–48.
Reid’s paradox revisited: the evolution of dispersal kernels during range expansion.CrossRef | open url image1

Posada, D., and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.
MODELTEST: testing the model of DNA substitution.CrossRef | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=49d1e8ce46168e568add0785b4abd1d2CAS | 9918953PubMed | open url image1

Reed, D. H., and Frankham, R. (2001). How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55, 1095–1103.
| 1:STN:280:DC%2BD38%2FisFWitA%3D%3D&md5=c42a7f3a1a9bbbd864a40c76ecbdb68aCAS | 11475045PubMed | open url image1

Reed, D. H., and Frankham, R. (2003). Correlation between fitness and genetic diversity. Conservation Biology 17, 230–237.
Correlation between fitness and genetic diversity.CrossRef | open url image1

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed models.CrossRef | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=544b296d48ad75d42c45092f433e09b6CAS | 12912839PubMed | open url image1

Schneider, C. J., Cunningham, M., and Moritz, C. (1998). Comparative phylogeography and the history of endemic vertebrates in the Wet Tropics rainforests of Australia. Molecular Ecology 7, 487–498.
Comparative phylogeography and the history of endemic vertebrates in the Wet Tropics rainforests of Australia.CrossRef | open url image1

Sinervo, B., Méndez-de-la-Cruz, F., Miles, D. B., Heulin, B., Bastiaans, E., Villagrán-Santa Cruz, M., Lara-Resendiz, R., Martínez-Méndez, N., Calderón-Espinosa, M. L., Meza-Lázaro, R. N., Gadsden, H., Avila, L. J., Morando, M., De la Riva, I. J., Sepulveda, P. V., Rocha, C. F. D., Ibargüengoytía, N., Puntriano, C. A., Massot, M., Lepetz, V., Oksanen, T. A., Chapple, D. G., Bauer, A. M., Branch, W. R., Clobert, J., and Sites, J. W. (2010). Erosion of lizard diversity by climate change and altered thermal niches. Science 328, 894–899.
Erosion of lizard diversity by climate change and altered thermal niches.CrossRef | 1:CAS:528:DC%2BC3cXlvVeltrY%3D&md5=eefc19c0acd58be53ca31ba0b3a6ecd0CAS | 20466932PubMed | open url image1

Slatkin, M., and Barton, N. H. (1989). A comparison of three indirect methods for estimating average levels of gene flow. Evolution 43, 1349–1368. open url image1

Strasburg, J. L., and Kearney, M. (2005). Phylogeography of sexual Heteronotia binoei (Gekkonidae) in the Australian arid zone: climatic cycling and repetitive hybridization. Molecular Ecology 14, 2755–2772.
Phylogeography of sexual Heteronotia binoei (Gekkonidae) in the Australian arid zone: climatic cycling and repetitive hybridization.CrossRef | 1:CAS:528:DC%2BD2MXpt1Cju74%3D&md5=d0e6fbd538a70796ed1b5359aabf06a4CAS | 16029476PubMed | open url image1

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA 5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA 5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.CrossRef | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=e841dcb65bf5743a3261692bb5310fe6CAS | 21546353PubMed | open url image1

Taubmann, J., Theissinger, K., Feldheim, K., Laube, I., Graf, W., Haase, P., Johannesen, J., and Pauls, S. (2011). Modelling range shifts and assessing genetic diversity distribution of the montane aquatic mayfly Ameletus inopinatus in Europe under climate change scenarios. Conservation Genetics 12, 503–515.
Modelling range shifts and assessing genetic diversity distribution of the montane aquatic mayfly Ameletus inopinatus in Europe under climate change scenarios.CrossRef | open url image1

Tavare, S. (1986). Some probabilistic and statistical problems in the analysis of DNA sequences. American Mathematical Society 17, 57–86. open url image1

Taylor, M., and Figgis, P. (2007). Protected Areas: buffering nature against climate change – overview and recommendations. In ‘Protected Areas: Buffering Nature Against Climate Change. Proceedings of a WWF and IUCN World Commission on Protected Areas Symposium, 18–19 June 2007, Canberra’. (Eds M. Taylor, and P. Figgis.) pp. 1–12. (WWF-Australia: Sydney.)

Thuiller, W., Lavorel, S., Araujo, M. B., Sykes, M. T., and Prentice, I. C. (2005). Climate change threats to plant diversity in Europe. Proceedings of the National Academy of Sciences of the United States of America 102, 8245–8250.
Climate change threats to plant diversity in Europe.CrossRef | 1:CAS:528:DC%2BD2MXlsV2mt7k%3D&md5=f1e4161589966b8974b2977d63e26c30CAS | 15919825PubMed | open url image1

Tol, R. (2005). Select Committee on Economic Affairs Minutes of Evidence (15 January 2005). “Memorandum by Professor Richard S J Tol, Hamburg, Vrije and Carnegie Mellon Universities. In (report): The Economics of Climate Change, the Second Report of the 2005–2006 session, produced by the UK Parliament House of Lords Economics Affairs Select Committee”. UK Parliament website. Accessed 2011-03-27.

Weeks, A. R., Sgro, C. M., Young, A. G., Frankham, R., Mitchell, N. J., Miller, K. A., Byrne, M., Coates, D. J., Eldridge, M. D. B., Sunnucks, P., Breed, M. F., James, E. A., and Hoffmann, A. A. (2011). Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evolutionary Applications 4, 709–725.
Assessing the benefits and risks of translocations in changing environments: a genetic perspective.CrossRef | 22287981PubMed | open url image1

Wright, S. (1943). Isolation by distance. Genetics 28, 114–138.
| 1:STN:280:DC%2BD2s%2FmsFSmsg%3D%3D&md5=491633a44fb61bb3f2a70f6fc4b2ee7aCAS | 17247074PubMed | open url image1

Wright, S. (1969). ‘Evolution and the Genetics of Populations. Volume 2. The Theory of Gene Frequencies.’ (University of Chicago Press: Chicago.)



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