Abstract
Sky islands are high-elevation areas in continental mountain ranges, which are geographically isolated. We adopted this concept for the mountains in southwest China, which are among the most important biodiversity hot spots on earth. We reviewed the phylogeographic studies of this area and highlighted the sky-island features. We concluded that the genetic structures of species in these islands were shaped by complex topography, climate and habitats. The global climate change, such as Pleistocene climate fluctuations and periodic uplift of the Qinghai–Tibetan Plateau, also have important effects on biodiversity and geographic patterns, when species have responded idiosyncratically by changing their distributions or through adaptation. Future research needs in sky islands include multilocus data and comparative phylogeographic studies, integrating with the methodological advances in the other fields. Using these approaches, we can examine to what degree the geographic, climate and/or biological factors, shape strong geographic patterns, promote diversification/speciation and preserve species/genetic diversity. We hope this paper will inspire future work to uncover the mechanism that has generated the endemic biodiversity and to further resolve the most essential problem: How to protect the biodiversity with limited funding during the coming drastic global climate change.
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References
Heald W (1951) Sky islands of Arizona. Nat Hist 60:56–63
Mclaughlin SP (1994) An overview of the flora of the Sky Islands, southeastern Arizona: diversity, affinities, and insularity. Biodiversity and management of the Madrean Archipelago: the Sky Islands of southwestern United States and northwestern Mexico, pp 60–70
Warshall P (1995) The Madrean sky island archipelago: a planetary overview. In: Debano LF, Gottfried GJ, Hamre RH et al (eds) Biodiversity and management of the Madrean Archipelago: the sky islands of southwestern United States and northwestern Mexico. US Department of Agriculture, Fort Collins, CO, pp 6–18
Hudson R, Slatkin M, Maddison W (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132:583
Knowles LL (2001) Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers. Mol Ecol 10:691–701
Dechaine EG, Martin AP (2004) Historic cycles of fragmentation and expansion in Parnassius smintheus (Papilionidae) inferred using mitochondrial DNA. Evolution 58:113–127
Dechaine EG, Martin AP (2005) Marked genetic divergence among sky island populations of Sedum lanceolatum (Crassulaceae) in the rocky mountains. Am J Bot 92:477–486
Coulon A, Cosson JF, Angibault JM et al (2004) Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual-based approach. Mol Ecol 13:2841–2850
Browne RA, Ferree PM (2007) Genetic structure of southern Appalachian “sky island” populations of the southern red-backed vole (Myodes gapperi). J Mammal 88:759–768
Hewitt G (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276
McCormack JE, Bowen BS, Smith TB (2008) Integrating paleoecology and genetics of bird populations in two sky island archipelagos. BMC Biol 6:28
Bowie RCK, Fjeldsa J, Hackett SJ et al (2006) Coalescent models reveal the relative roles of ancestral polymorphism, vicariance, and dispersal in shaping phylogeographical structure of an African montane forest robin. Mol Phylogenet Evol 38:171–188
Downie DA (2004) Phylogeography in a galling insect, grape phylloxera, Daktulosphaira vitifoliae (Phylloxeridae) in the fragmented habitat of the Southwest USA. J Biogeogr 31:1759–1768
Fu Y (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915
Harpending H (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol Int Rec Res 66:591
Drummond AJ, Rambaut A, Shapiro B et al (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192
Wiens JJ (2004) Speciation and ecology revisited: Phylogenetic niche conservatism and the origin of species. Evolution 58:193–197
Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annu Rev Ecol Evol Syst 36:519–539
Mccormack JE, Smith TB (2008) Niche expansion leads to small-scale adaptive divergence along an elevation gradient in a medium-sized passerine bird. Proc R Soc B Biol Sci 275:2155–2164
Masta SE, Maddison WP (2002) Sexual selection driving diversification in jumping spiders. Proc Natl Acad Sci USA 99:4442–4447
Mccormack J, Huang H, Knowle L (2009) Sky islands. In: Gillespie RG, Clague DA (eds) Encyclopedia of Islands. University of California Press, Berkeley, CA, pp 841–843
Zhao E, Yang D (1997) Amphibians and reptiles of the Hengduan Mountain region. Science Press, Beijing
Guo P, Liu Q, Li C et al (2011) Molecular phylogeography of Jerdon’s pitviper (Protobothrops jerdonii): importance of the uplift of the Tibetan plateau. J Biogeogr 38:2326–2336
Qu YH, Luo X, Zhang RY et al (2011) Lineage diversification and historical demography of a montane bird Garrulax elliotii—implications for the Pleistocene evolutionary history of the eastern Himalayas. BMC Evol Biol 11:174
Qin L, Meng X-M, Kryukov AP et al (2007) Species and distribution patterns of small mammals in the Pingheliang Nature Reserve of Qinling Mountain, Shaanxi. Zool Res 28:231–242
Li Y, Xu L, Ma Y et al (2003) The species richness of nonvolant mammals in Shennongjia Nature Reserve, Hubei Province, China: distribution patterns along elevational gradient. Biodivers Sci 11:1–9
Zhao C, Wang CB, Ma XG et al (2013) Phylogeographic analysis of a temperate-deciduous forest restricted plant (Bupleurum longiradiatum Turcz.) reveals two refuge areas in China with subsequent refugial isolation promoting speciation. Mol Phylogenet Evol 68:628–643
Zhang DC, Boufford DE, Ree RH et al (2009) The 29°N latitudinal line: an important division in the Hengduan mountains, a biodiversity hotspot in southwest China. Nordic J Bot 27:405–412
He D, Li S, Zhang Y (2007) The variation and regional differences of precipitation in the Longitudinal Range-Gorge the Region. Chin Sci Bull 52:59–73
Li BY (1989) Geomorphologic regionalization of the Hengduan Mountainous region. J Mt Res 7:13–20
Li XW, Li J (1993) A preliminary floristic study on the seed plants from the region of Hengduan Mountain. Acta Bot Yunnanica 15:217–231
Yao Y, Zhang B, Han F et al (2010) Diversity and geographical pattern of altitudinal belts in the Hengduan Mountains in China. J Mt Sci 7:123–132
Myers N, Mittermeier R, Mittermeier C et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Zhang RZ (2002) Geological events and mammalian distribution in China. Acta Zool Sin 48:141–153
Zhang R-Z (1997) Distribution of mammalian species in China. China Forestry Publishing House, Beijing
Li J, He QX, Hua X et al (2009) Climate and history explain the species richness peak at mid-elevation for Schizothorax fishes (Cypriniformes: Cyprinidae) distributed in the Tibetan Plateau and its adjacent regions. Glob Ecol Biogeogr 18:264–272
Zhang M, Rao D, Yang J et al (2010) Molecular phylogeography and population structure of a mid-elevation montane frog Leptobrachium ailaonicum in a fragmented habitat of southwest China. Mol Phylogenet Evol 54:47–58
Liu Q, Chen P, He K et al (2012) Phylogeographic Study of Apodemus ilex (Rodentia: Muridae) in Southwest China. PLoS ONE 7:e31453
Fan Z, Liu S, Liu Y et al (2012) Phylogeography of the South China field mouse (Apodemus draco) on the Southeastern tibetan plateau reveals high genetic diversity and glacial refugia. PLoS ONE 7:e38184
Yang ZY, Yi TS, Pan YZ et al (2012) Phylogeography of an alpine plant Ligularia vellerea (Asteraceae) in the Hengduan Mountains. J Syst Evol 50:316–324
Zhu L, Zhan X, Meng T et al (2010) Landscape features influence gene flow as measured by cost-distance and genetic analyses: a case study for giant pandas in the Daxiangling and Xiaoxiangling Mountains. BMC Genet 11:72
Yang FS, Qin AL, Li YF et al (2012) Great genetic differentiation among populations of Meconopsis integrifolia and its implication for plant speciation in the Qinghai-Tibetan plateau. PLoS ONE 7
Zhang TC, Comes HP, Sun H (2011) Chloroplast phylogeography of Terminalia franchetii (Combretaceae) from the eastern Sino-Himalayan region and its correlation with historical river capture events. Mol Phylogenet Evol
Clark M, Schoenbohm L, Royden L et al (2004) Surface uplift, tectonics, and erosion of eastern Tibet from large-scale drainage patterns. Tectonics 23:1006–1029
Cheng J, Liu X, Gao Z et al (2001) Effect of the Tibetan Plateau uplifting on the geological environment of the Yunnan Plateau. Geoscience 15:290–296
Pan T, Wu S, He D et al (2012) Effects of longitudinal range-gorge terrain on the eco-geographical pattern in Southwest China. J Geog Sci 22:825–842
Chen SD, Liu SY, Liu Y et al (2012) Molecular phylogeny of asiatic short-tailed shrews, genus Blarinella Thomas, 1911 (Mammalia: Soricomorpha: Soricidae) and its taxonomic implications. Zootaxa 3250:43–53
Li R, Chen W, Tu L et al (2009) Rivers as barriers for high elevation amphibians: a phylogeographic analysis of the alpine stream frog of the Hengduan Mountains. J Zool 277:309–316
Zhang DR, Chen MY, Murphy RW et al (2010) Genealogy and palaeodrainage basins in Yunnan Province: phylogeography of the Yunnan spiny frog, Nanorana yunnanensis (Dicroglossidae). Mol Ecol 19:3406–3420
Chung SL, Lo CH, Lee TY et al (1998) Diachronous uplift of the Tibetan plateau starting 40 Myr ago. Nature 394:769–773
Wu FY, Huang BC, Ye K et al (2008) Collapsed Himalayan-Tibetan orogen and the rising Tibetan Plateau. Acta Petrol Sin 24:1–30
Li J, Fang X (1999) Uplift of the Tibetan Plateau and environmental changes. Chin Sci Bull 44:2117–2124
Liu J-Q, Wang Y-J, Wang A-L et al (2006) Radiation and diversification within the Ligularia–Cremanthodium–Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau. Mol Phylogenet Evol 38:31–49
Liu J-Q, Gao T-G, Chen Z-D et al (2002) Molecular phylogeny and biogeography of the Qinghai-Tibet Plateau endemic Nannoglottis (Asteraceae). Mol Phylogenet Evol 23:307–325
Clift PD, Blusztajn J, Duc NA (2006) Large-scale drainage capture and surface uplift in eastern Tibet-SW China before 24 Ma inferred from sediments of the Hanoi Basin, Vietnam. Geophys Res Lett 33:L19403
Molnar P, England P, Martinod J (1993) Mantle dynamics, uplift of the Tibetan Plateau, and the Indian monsoon. Rev Geophys 31:357–396
Peng ZG, Ho SYW, Zhang YG et al (2006) Uplift of the Tibetan plateau: evidence from divergence times of glyptosternoid catfishes. Mol Phylogenet Evol 39:568–572
Che J, W-W Zhou, J-S Hu et al (2010) Spiny frogs (Paini) illuminate the history of the Himalayan region and Southeast Asia. Proc Natl Acad Sci USA 107:13765–13770
He DK, Chen YF (2006) Biogeography and molecular phylogeny of the genus Schizothorax (Teleostei: Cyprinidae) in China inferred from cytochrome b sequences. J Biogeogr 33:1448–1460
Zhang TC, Comes HP, Sun H (2011) Chloroplast phylogeography of Terminalia franchetii (Combretaceae) from the eastern Sino-Himalayan region and its correlation with historical river capture events. Mol Phylogenet Evol 60:1–12
Zhao X, Qu Y, Zhang Y et al (2007) Discovery of Shigu paleolake in the Lijiang area, northwestern Yunnan, China and its significance for the development of the modern Jinsha River valley. Geol Bull China 26:960–969
Bennett KD (1990) Milankovitch cycles and their effects on species in ecological and evolutionary time. Paleobiology 16:11–21
Zachos J, Pagani M, Sloan L et al (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693
An Z, Kutzbach JE, Prell WL et al (2001) Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times. Nature 411:62–66
Qiu ZD, Li CK (2005) Evolution of Chinese mammalian faunal regions and elevation of the Qinghai-Xizang (Tibet) Plateau. Sci China Ser D Earth Sci 48:1246–1258
Qiang XK, Li ZX, Powell CM et al (2001) Magnetostratigraphic record of the Late Miocene onset of the East Asian monsoon, and Pliocene uplift of northern Tibet. Earth Planet Sci Lett 187:83–93
Jia G, Peng P, Zhao Q et al (2003) Changes in terrestrial ecosystem since 30 Ma in East Asia: stable isotope evidence from black carbon in the South China Sea. Geology 31:1093–1096
Xu X, Fang X (2008) Rock magnetic record of Cenozoic lake sediments from the Linxia basin and aridification of the Asian inland. Front Earth Sci China 2:217–224
He K, Li YJ, Brandley MC et al (2010) A multi-locus phylogeny of Nectogalini shrews and influences of the paleoclimate on speciation and evolution. Mol Phylogenet Evol 56:734–746
Li ZJ, Yu GH, Rao DQ et al (2012) Phylogeography and demographic history of Babina pleuraden (Anura, Ranidae) in southwestern China. PLoS ONE 7:e34013
Xie X-F, Yan H-F, Wang F-Y et al (2012) Chloroplast DNA phylogeography of Primula ovalifolia in central and adjacent southwestern China: past gradual expansion and geographical isolation. J Syst Evol 50:284–294
Hewitt G (2004) Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond B Biol Sci 359:183–195
Soltis DE, Morris AB, Mclachlan JS et al (2006) Comparative phylogeography of unglaciated eastern North America. Mol Ecol 15:4261–4293
Hewitt G (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112
Rull V (2009) Microrefugia. J Biogeogr 36:481–484
Gomez A, Lunt DH (2007) Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In: Phylogeography in southern European refugia: evolutionary perspectives on the origins and conservation of European biodiversity. Dordrecht: Kluwer Academic Publishers, pp 155–188
Igea J, Aymerich P, Fernandez-Gonzalez A et al (2013) Phylogeography and postglacial expansion of the endangered semi-aquatic mammal Galemys pyrenaicus. BMC Evol Biol 13:115
Yu G, Zhang M, Rao D et al (2013) Effect of pleistocene climatic oscillations on the phylogeography and demography of red knobby newt (Tylototriton shanjing) from Southwestern China. PLoS ONE 8:e56066
Yan F, Zhou WW, Zhao HT et al (2013) Geological events play a larger role than Pleistocene climatic fluctuations in driving the genetic structure of Quasipaa boulengeri (Anura: Dicroglossidae). Mol Ecol 22:1120–1133
Fazalova V, Nevado B, Peretolchina T et al (2010) When environmental changes do not cause geographic separation of fauna: differential responses of Baikalian invertebrates. BMC Evol Biol 10:320
Wu CH, Li HP, Wang YX et al (2000) Low genetic variation of the Yunnan hare (Lepus comus G. Allen 1927) as revealed by mitochondrial cytochrome b gene sequences. Biochem Genet 38:147–153
Zhao S, Zheng P, Dong S et al (2013) Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nat Genet 45:67–71
Bennett KD, Provan J (2008) What do we mean by ‘refugia? Quatern Sci Rev 27:2449–2455
Zhou TH, Li S, Qian ZQ et al (2010) Strong phylogeographic pattern of cpDNA variation reveals multiple glacial refugia for Saruma henryi Oliv. (Aristolochiaceae), an endangered herb endemic to China. Mol Phylogenet Evol 57:176–188
Liu JQ, Sun YS, Ge XJ et al (2012) Phylogeographic studies of plants in China: advances in the past and directions in the future. J Syst Evol 50:267–275
Ponniah M, Hughes J (2004) The evolution of Queensland spiny mountain crayfish of the genus Euastacus. I. Testing vicariance and dispersal with interspecific mitochondrial DNA. Evolution 58:1073–1085
Irwin DE, Bensch S, Price TD (2001) Speciation in a ring. Nature 409:333–337
Monahan W, Pereira R, Wake D (2012) Ring distributions leading to species formation: a global topographic analysis of geographic barriers associated with ring species. BMC Biol 10:20
Toews DP, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930
Brito P, Edwards SV (2009) Multilocus phylogeography and phylogenetics using sequence-based markers. Genetica 135:439–455
Emerson KJ, Merz CR, Catchen JM et al. (2010) Resolving postglacial phylogeography using high-throughput sequencing. In: Proceedings of the national academy of sciences, 2010, vol 107, pp 16196–16200
Davey JW, Hohenlohe PA, Etter PD et al (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510
Cronn R, Knaus BJ, Liston A et al (2012) Targeted enrichment strategies for next-generation plant biology. Am J Bot 99:291–311
O’neill EM, Schwartz R, Bullock CT et al (2013) Parallel tagged amplicon sequencing reveals major lineages and phylogenetic structure in the North American tiger salamander (Ambystoma tigrinum) species complex. Mol Ecol 22:111–129
McCormack JE, Faircloth BC (2013) Next-generation phylogenetics takes root. Mol Ecol 22:19–21
Avise JC, Arnold J, Ball RM et al (1987) Intraspecific phylogeography—the mitochondrial-DNA bridge between population-genetics and systematics. Annu Rev Ecol Syst 18:489–522
Knowles LL (2009) Statistical phylogeography. Annu Rev Ecol Evol Syst 40:593–612
Hickerson MJ, Carstens BC, Cavender-Bares J et al (2010) Phylogeography’s past, present, and future: 10 years after Avise, 2000. Mol Phylogenet Evol 54:291–301
Nielsen R, Beaumont MA (2009) Statistical inferences in phylogeography. Mol Ecol 18:1034–1047
Bell RC, Mackenzie JB, Hickerson MJ et al (2012) Comparative multi-locus phylogeography confirms multiple vicariance events in co-distributed rainforest frogs. Proc R Soc B Biol Sci 279:991–999
Carstens BC, Richards CL (2007) Integrating coalescent and ecological niche modeling in comparative phylogeography. Evolution 61:1439–1454
Elith J, Phillips SJ, Hastie T et al (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57
Knowles LL, Carstens BC, Keat ML (2007) Coupling genetic and ecological-niche models to examine how past population distributions contribute to divergence. Curr Biol 17:940–946
Scoble J, Lowe AJ (2010) A case for incorporating phylogeography and landscape genetics into species distribution modelling approaches to improve climate adaptation and conservation planning. Divers Distrib 16:343–353
Yang Z, Rannala B (2010) Bayesian species delimitation using multilocus sequence data. Proc Natl Acad Sci USA 107:9264
Zelditch M (2004) Geometric morphometrics for biologists: a primer. Academic Press, London
Joost S, Bonin A, Bruford MW et al (2007) A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Mol Ecol 16:3955–3969
Dai Z, Du J, Li J et al (2008) Runoff characteristics of the Changjiang River during 2006: effect of extreme drought and the impounding of the Three Gorges Dam. Geophys Res Lett 35:L07406
Provan J, Maggs CA (2012) Unique genetic variation at a species’ rear edge is under threat from global climate change. Proc R Soc B Biol Sci 279:39–47
Pfenninger M, Balint M, Pauls S (2012) Methodological framework for projecting the potential loss of intraspecific genetic diversity due to global climate change. BMC Evol Biol 12:224
Bottrill MC, Joseph LN, Carwardine J et al (2008) Is conservation triage just smart decision making? Trends Ecol Evol 23:649–654
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31272276), the Key Research Program of the Chinese Academy of Science (KJZD-EW-L07) and the State Key Laboratory of Genetics Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences (GREKF11-03). We appreciate the three anonymous reviewers for their critical reviews and valuable suggestions. We thank Dr. John McCormack and Dr. Gina C. Gould for providing valuable comments and suggestions, as well as English editing which improved the quality of this manuscript. We thank Feng Dong and Guo-Hua Yu for discussion on an earlier draft of the manuscript. We also thank John McCormack, Zhenxin Fan, Dongru Zhang and Fusheng Yang for allowing us to reproduce the figures in their paper.
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He, K., Jiang, X. Sky islands of southwest China. I: an overview of phylogeographic patterns. Chin. Sci. Bull. 59, 585–597 (2014). https://doi.org/10.1007/s11434-013-0089-1
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DOI: https://doi.org/10.1007/s11434-013-0089-1