Abstract
Understanding how species have responded to strong climatic fluctuations accompanying glacial-interglacial cycles is critical to predicting their likely responses to future climate change, and therefore can help guide conservation strategies. Using molecular phylogeography and ecological niche modelling, we aimed to understand how a newly recognized cryptic montane mammal (Spermophilus taurensis, Taurus ground squirrels) has responded to global climate changes through the Late Quaternary glacial-interglacial cycles as a means to better predict their likely responses to future climate change. Accordingly, 51 cytochrome b mitochondrial DNA sequences from throughout the known distribution of Taurus ground squirrels were used to investigate the intraspecific diversification. Besides molecular phylogeography, ecological niche modelling was also employed to get insights into possible climate-driven altitudinal range shifts in the past (the Last Glacial Maximum, 22 kya and the Mid-Holocene, 6 kya) and in the future (2050). Taurus ground squirrels survived the Late Quaternary glacial-interglacial cycles by altitudinal migrations without large geographical displacements. As warming occurred from the Last Glacial Maximum to the Mid-Holocene to the present, the potential distribution of Taurus ground squirrels shifted towards higher altitudes, resulting in a smaller range in the present. As warming continues, the potential distribution of Taurus ground squirrels will continue to shift towards higher altitudes, resulting in a much smaller range in the future. Particular sources of concern are the synergistic effects of future climate change and anthropogenic impacts on Taurus ground squirrels and their montane environments.
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References
Agassiz L (1840) Études sur les glaciers (Studies of glaciers). Jent and Gassmann, Neuchâtel
Alvarado-Serrano DF, Knowles LL (2014) Ecological niche models in phylogeographic studies: applications, advances and precautions. Mol Ecol Resour 14(2):233–248. https://doi.org/10.1111/1755-0998.12184
Arslan E, Arslan A (2010) Heterochromatin distribution and nucleolar organizer regions (NORs) in chromosomes of the Taurus ground squirrel, Spermophilus taurensis Gündüz et al., 2007 (Mammalia: Rodentia), in Turkey. Turk J Zool 34:105–110
Avcı M (2005) Çeşitlilik ve endemizm açısından Türkiye'nin bitki örtüsü (Diversity and Endemism in Turkey’s Vegetation). Coğrafya Dergisi 13:27–55
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Bennett KD, Provan J (2008) What do we mean by ‘refugia’? Quat Sci Rev 27(27-28):2449–2455. https://doi.org/10.1016/j.quascirev.2008.08.019
Boria RA, Olson LE, Goodman SM, Anderson RP (2014) Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol Model 275:73–77. https://doi.org/10.1016/j.ecolmodel.2013.12.012
Brown JL (2014) SDMtoolbox: a python-based GIS toolkit for landscape genetic, biogeographic and species distribution model analyses. Methods Ecol Evol 5(7):694–700. https://doi.org/10.1111/2041-210X.12200
Brown JL, Weber JJ, Alvarado-Serrano DF, Hickerson MJ, Franks SJ, Carnaval AC (2016) Predicting the genetic consequences of future climate change: the power of coupling spatial demography, the coalescent, and historical landscape changes. Am J Bot 103(1):153–163. https://doi.org/10.3732/ajb.1500117
Brunhoff C, Galbreath KE, Fedorov VB, Cook JA, Jaarola, M (2003) Holarctic phylogeography of the root vole (Microtus oeconomus): implications for late Quaternary biogeography of high latitudes. Mol Ecol 12(4):957–968
Chan LM, Brown JL, Yoder AD (2011) Integrating statistical genetic and geospatial methods brings new power to phylogeography. Mol Phylogenet Evol 59(2):523–537. https://doi.org/10.1016/j.ympev.2011.01.020
Çiner A, Sarıkaya MA, Yıldırım C (2015) Late Pleistocene piedmont glaciations in the eastern Mediterranean; insights from cosmogenic 36Cl dating of hummocky moraines in southern Turkey. Quat Sci Rev 116:44–56. https://doi.org/10.1016/j.quascirev.2015.03.017
Davis PH (1971) Distribution patterns in Anatolia with particular reference to endemism. In: Davis PH, Harper PC, Hedge IC (eds) Plant life of South-West Asia. Botanical Society of Edinburgh, Edinburgh, pp 15–27
Ditto AM, Frey JK (2007) Effects of ecogeographic variables on genetic variation in montane mammals: implications for conservation in a global warming scenario. J Biogeogr 34(7):1136–1149. https://doi.org/10.1111/j.1365-2699.2007.01700.x
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29(8):1969–1973. https://doi.org/10.1093/molbev/mss075
Edwards SV, Shultz AJ, Campbell-Staton SC (2015) Next-generation sequencing and the expanding domain of phylogeography. Folia Zool 64:187–206
Elith J, Leathwick JR (2009a) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Syst 40(1):677–697. https://doi.org/10.1146/annurev.ecolsys.110308.120159
Elith J, Leathwick JR (2009b) The contribution of species distribution modelling to conservation prioritization. In: Moilanen A, Wilson KA, Possingham HP (eds) Spatial conservation prioritization: quantitative methods and computational tools. Oxford University Press, Oxford, pp 70–93
Elith J, Graham C, Anderson R et al (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29(2):129–151. https://doi.org/10.1111/j.2006.0906-7590.04596.x
Elith J, Kearney M, Phillips S (2010) The art of modelling range-shifting species. Methods Ecol Evol 1(4):330–342. https://doi.org/10.1111/j.2041-210X.2010.00036.x
Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17(1):43–57. https://doi.org/10.1111/j.1472-4642.2010.00725.x
Feldman RE, Peers MJ, Pickles RS, Thornton D, Murray DL (2017) Climate driven range divergence among host species affects range-wide patterns of parasitism. Glob Ecol Conserv 9:1–10. https://doi.org/10.1016/j.gecco.2016.10.001
Galbreath KE, Hafner DJ, Zamudio KR (2009) When cold is better: climate-driven elevation shifts yield complex patterns of diversification and demography in an alpine specialist (American pika, Ochotona princeps). Evolution 63(11):2848–2863. https://doi.org/10.1111/j.1558-5646.2009.00803.x
Graham RW (1986) Response of mammalian communities to environmental changes during the late quaternary. In: Diamond J, Case TJ (eds) Community ecology. Harper and Row, New York, pp 300–313
Gündüz İ, Jaarola M, Tez C, Yeniyurt C, Polly PD, Searle JB (2007) Multigenic and morphometric differentiation of ground squirrels (Spermophilus, Scuiridae, Rodentia) in Turkey, with a description of a new species. Mol Phylogenet Evol 43(3):916–935. https://doi.org/10.1016/j.ympev.2007.02.021
Gür H (2013) The effects of the late quaternary glacial–interglacial cycles on Anatolian ground squirrels: range expansion during the glacial periods? Biol J Linn Soc 109(1):19–32. https://doi.org/10.1111/bij.12026
Gür H (2016) The Anatolian diagonal revisited: testing the ecological basis of a biogeographic boundary. Zool Middle East 62(3):189–199. https://doi.org/10.1080/09397140.2016.1226544
Gür H, Kart Gür M (2005) Annual cycle of activity, reproduction, and body mass of Anatolian ground squirrels (Spermophilus xanthoprymnus) in Turkey. J Mammal 86(1):7–14. https://doi.org/10.1644/1545-1542(2005)086<0007:ACOARA>2.0.CO;2
Gür H, Kart Gür M (2012) Is spatial variation in food availability an explanation for a Bergmannian size pattern in a North American hibernating, burrowing mammal? An information-theoretic approach. J Zool 287(2):104–114. https://doi.org/10.1111/j.1469-7998.2011.00893.x
Harrison S, Viers JH, Quinn JF (2000) Climatic and spatial patterns of diversity in serpentine plants of California. Divers Distrib 6(3):153–161. https://doi.org/10.1046/j.1472-4642.2000.00082.x
Helgen KM, Cole FR, Helgen LE, Wilson DE (2009) Generic revision in the Holarctic ground squirrel genus Spermophilus. J Mammal 90(2):270–305. https://doi.org/10.1644/07-MAMM-A-309.1
Hernandez PA, Graham CH, Master LL, Albert DL (2006) The effect of sample size and species characteristics on performance of different species distribution modeling methods. Ecography 29(5):773–785
Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405(6789):907–913. https://doi.org/10.1038/35016000
Hewitt GM (2004a) Genetic consequences of climatic oscillations in the quaternary. Philos Trans R Soc B 359(1442):183–195. https://doi.org/10.1098/rstb.2003.1388
Hewitt GM (2004b) The structure of biodiversity–insights from molecular phylogeography. Front Zool 1:1
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25(15):1965–1978. https://doi.org/10.1002/joc.1276
Hughes PD, Woodward JC (2017) Quaternary glaciation in the Mediterranean mountains: a new synthesis. In: Hughes PD, Woodward JC (ed) Quaternary glaciation in the Mediterranean region. Geological Society, London, Special Publications, 433, pp 1–23, 1. https://doi.org/10.1144/SP433.14
Jansen E, Overpeck J, Briffa KR et al (2007) Palaeoclimate. In: Solomon S, Qin D, Manning M et al (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 433–497
Jansson R, Dynesius M (2002) The fate of clades in a world of recurrent climatic change: Milankovitch oscillations and evolution. Annu Rev Ecol Syst 33(1):741–777. https://doi.org/10.1146/annurev.ecolsys.33.010802.150520
Jiménez-Valverde A, Nakazawa Y, Lira-Noriega A, Peterson AT (2009) Environmental correlation structure and ecological niche model projections. Biodivers Inform 6:28–35
Johnston KM, Freund KA, Schmitz OJ (2012) Projected range shifting by montane mammals under climate change: implications for Cascadia’s National Parks. Ecosphere 3:1–51
Kart Gür M, Gür H (2010) Spermophilus xanthoprymnus (Rodentia: Sciuridae). Mamm Species 42:183–194
Kart Gür M, Gür H (2015) Age and sex differences in hibernation patterns in free-living Anatolian ground squirrels. Mamm Biol 80(4):265–272. https://doi.org/10.1016/j.mambio.2015.02.006
Kryštufek B, Yigit N, Hutterer R (2008) Spermophilus xanthoprymnus. The IUCN red list of threatened species 2008: e.T20496A9209216. https://doi.org/10.2305/IUCN.UK.2008.RLTS.T20496A9209216.en . Downloaded on 02 December 2016
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evo 6(9):1110–1116. https://doi.org/10.1111/2041-210X.12410
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452. https://doi.org/10.1093/bioinformatics/btp187
López-Pujol J, López-Vinyallonga S, Susanna A, Ertuğrul K, Uysal T, Tugay O, Guetat A, Garcia-Jacas N (2016) Speciation and genetic diversity in Centaurea subsect. Phalolepis in Anatolia. Sci Rep 6(1):37818. https://doi.org/10.1038/srep37818
Médail F, Diadema K (2009) Glacial refugia influence plant diversity patterns in the Mediterranean basin. J Biogeogr 36(7):1333–1345. https://doi.org/10.1111/j.1365-2699.2008.02051.x
Médail F, Quezel P (1997) Hot-spots analysis for conservation of plant biodiversity in the Mediterranean Basin. Ann Mo Bot Gard 84(1):112–127. https://doi.org/10.2307/2399957
Merow C, Smith MJ, Silander JA (2013) A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36(10):1058–1069. https://doi.org/10.1111/j.1600-0587.2013.07872.x
Mittermeier RA, Gil PR, Hoffman M et al (2004) Hotspots revisited. CEMEX, Mexico
Morelli TL, Smith AB, Kastely CR, Mastroserio I, Moritz C, Beissinger SR (2012) Anthropogenic refugia ameliorate the severe climate-related decline of a montane mammal along its trailing edge. Proc R Soc Lond B 279(1745):4279–4286. https://doi.org/10.1098/rspb.2012.1301
Nielsen R, Wakeley JW (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896
Özkurt ŞÖ, Sözen M, Yiğit N, Kandemir İ, Çolak R, Gharkheloo MM, Çolak E (2007) Taxonomic status of the genus Spermophilus (Mammalia: Rodentia) in Turkey and Iran with description of a new species. Zootaxa 1529(1):1–15. 10.11646/zootaxa.1529.1.1
Özüdoğru B, Akaydın G, Erik S, Al-Shehbaz IA, Mummenhoff K (2015) Phylogeny, diversification and biogeographic implications of the eastern Mediterranean endemic genus Ricotia (Brassicaceae). Taxon 64(4):727–740
Pabijan M, Brown JL, Chan LM, Rakotondravony HA, Raselimanana AP, Yoder AD, Glaw F, Vences M (2015) Phylogeography of the arid-adapted Malagasy bullfrog, Laliostoma Labrosum, influenced by past connectivity and habitat stability. Mol Phylogenet Evol 92:11–24. https://doi.org/10.1016/j.ympev.2015.05.018
PAGES (Past Interglacials Working Group of PAGES) (2016) Interglacials of the last 800,000 years. Rev Geophys 54(1):162–219. https://doi.org/10.1002/2015RG000482
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Syst 37(1):637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Parolly G (2015) The high-mountain flora and vegetation of the western and central Taurus Mts. (Turkey) in the times of climate change. In: Öztürk M, Hakeem KR, Faridah-Hanum I, Efe R (eds) Climate change impacts on high-altitude ecosystems. Springer International Publishing, Switzerland, pp 99–133
Peakall R, Smouse PE (2012) GenAIEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28(19):2537–2539
Perktaş U, Gür H (2015) Guest editors’ introduction to the special issue: integrating phylogeography and ecological niche modelling. Folia Zool 64:185–186
Perktaş U, Gür H, Ada E (2015) Historical demography of the Eurasian green woodpecker: integrating phylogeography and ecological niche modelling to test glacial refugia hypothesis. Folia Zool 64:284–295
Peterson AT, Anamza T (2015) Ecological niches and present and historical geographic distributions of species: a 15-year review of frameworks, results, pitfalls, and promises. Folia Zool 64:207–217
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190(3-4):231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Posada D, Crandall KA (2001) Selecting models of nucleotide substitution: an application to human immunodeficiency virus 1 (HIV-1). Mol Biol Evol 18(6):897–906. https://doi.org/10.1093/oxfordjournals.molbev.a003890
Qiao H, Soberón J, Escobar LE, Campbell L, Peterson AT (2015) NicheA. Version 3.0.1. Available at: http://nichea.sourceforge.net/
Rambaut A (2014) FigTree. Version 1.4.2. University of Edinburgh, Edinburgh, UK. Available at: http://tree.bio.ed.ac.uk/software/figtree/
Rambaut A, Drummond AJ (2009) Tracer v 1.5. Available at: http://tree.bio.ed.ac.uk/software/tracer/
Říčanová Š, Koshev Y, Říčan O, Ćosić N, Ćirović D, Sedláček F, Bryja J (2013) Multilocus phylogeography of the European ground squirrel: cryptic interglacial refugia of continental climate in Europe. Mol Ecol 22(16):4256–4269. https://doi.org/10.1111/mec.12382
Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421(6918):57–60. https://doi.org/10.1038/nature01333
Sarıkaya MA, Çiner A (2015) Late Pleistocene glaciations and paleoclimate of Turkey. Bulletin of the mineral. Res Explor 151:107–127
Sarıkaya MA, Çiner A (2017) Late quaternary glaciations in the eastern Mediterranean. In: Hughes PD, Woodward JC (ed) Quaternary glaciation in the Mediterranean region. Geological Society, London, Special Publications, 433, pp 289–305. 1. DOI: https://doi.org/10.1144/SP433.4
Sarıkaya MA, Çiner A, Zreda M (2011) Quaternary glaciations of Turkey. In: Ehlers J, Gibbard PL, Hughes PD (eds) Quaternary glaciations-extent and chronology, a closer look. Elsevier, Amsterdam, pp 393–403. https://doi.org/10.1016/B978-0-444-53447-7.00030-1
Şengör AMC, Yılmaz Y (1981) Tethyan evolution of Turkey—a plate tectonic approach. Tectonophysics 75(3-4):181–241. https://doi.org/10.1016/0040-1951(81)90275-4
Sevgili H, Çıplak B, Heller KG, Demirsoy A (2006) Morphology, bioacoustics and phylogeography of the Isophya major group (Orthoptera: Tettigoniidae: Phaneropterinae): A species complex occurring in Anatolia and Cyprus. Eur J Entomol 103(3):657–671
Stewart JR, Lister AM, Barnes I, Dalén L (2010) Refugia revisited: individualistic responses of species in space and time. Proc R Soc Lond B 277(1682):661–671. https://doi.org/10.1098/rspb.2009.1272
Thompson JD (2005) Plant evolution in the Mediterranean. Oxford University Press, New York. https://doi.org/10.1093/acprof:oso/9780198515340.001.0001
Thorington RW, Koprowski JL, Steele MA, Whatton JF (2012) Squirrels of the world. The Johns Hopkins University Press, Baltimore
Vandergast AG, Perry WM, Lugo RV, Hathaway SA (2011) Genetic landscapes GIS toolbox: tools to map patterns of genetic divergence and diversity. Mol Ecol Resour 11(1):158–161. https://doi.org/10.1111/j.1755-0998.2010.02904.x
Waltari E, Guralnick RP (2009) Ecological niche modelling of montane mammals in the Great Basin, North America: examining past and present connectivity of species across basins and ranges. J Biogeogr 36(1):148–161. https://doi.org/10.1111/j.1365-2699.2008.01959.x
Warren DL, Glor RE, Turelli M (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33:607–611
Welch H, Kirwan GM (2008) Turkey’s ecoregions: their biodiversity and conservation. In: Kirwan G, Demirci B, Welch H, Boyla K, Özen M, Castell P, Marlow T (eds) The birds of Turkey. Christopher Helm, London, pp 31–41
Wisz MS, Hijmans RJ, Li J, Peterson AT, Graham CH, Guisan A, NCEAS Predicting Species Distributions Working Group† (2008) Effects of sample size on the performance of species distribution models. Divers Distrib 14(5):763–773. https://doi.org/10.1111/j.1472-4642.2008.00482.x
Acknowledgments
We would like to thank M. Çakır, M. Çelik, H. Sevgili, and H. Yılmaz for sharing their field observations. This study was supported by the Ahi Evran University Scientific Research Projects Coordination Unit (Project Number: PYO-FEN.4001.15.008).
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U.P. conducted laboratory studies; H.G. conducted ecological niche modelling analyses; H.G and U.P. conducted molecular phylogeography analyses; H.G, U.P., and M.K.G. contributed to the interpretations of the results; and H.G. prepared and edited the manuscript, with input from all authors.
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Communicated by: Jan M. Wójcik
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S1 Figure
Marginal response curves of the bioclimatic variables (winter temperature and precipitation) that most contributed to the model. (GIF 49 kb)
S2 Figure
Bioclimatic niches of the northern and southern lineages (green and yellow, respectively). (GIF 53 kb)
S3 Figure
The posterior estimates of the parameters of theta (A), migration rate (B), and time to divergence (C) between the northern and southern populations. (GIF 35 kb)
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Gür, H., Perktaş, U. & Gür, M.K. Do climate-driven altitudinal range shifts explain the intraspecific diversification of a narrow ranging montane mammal, Taurus ground squirrels?. Mamm Res 63, 197–211 (2018). https://doi.org/10.1007/s13364-017-0347-8
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DOI: https://doi.org/10.1007/s13364-017-0347-8