Landscape Ecology

, Volume 28, Issue 9, pp 1729–1741 | Cite as

Effects of climatic gradients on genetic differentiation of Caragana on the Ordos Plateau, China

  • Jiuyan Yang
  • Samuel A. Cushman
  • Jie Yang
  • Mingbo Yang
  • Tiejun Bao
Research Article


The genus Caragana (Fabr.) in the Ordos Plateau of Inner Mongolia, China, provides a strong opportunity to investigate patterns of genetic differentiation along steep climatic gradients, and to identify the environmental factors most likely to be responsible for driving the radiation. This study used a factorial, multi-model approach to evaluate alternative hypotheses and identify the combination of environmental factors that appear to drive genetic divergence of Caragana in the Ordos Plateau. We had three specific hypotheses. First, we expected that gradients of changing climate would act as resistant factors limiting gene flow, and would provide stronger prediction of genetic differentiation than isolation by distance. Second, we expected that variation in precipitation would be a stronger predictor of genetic differentiation among populations than variation in temperature. Third, we expected that the pattern of phylogenetic differences, in terms of derived versus ancestral states of rachis and leaf shape, would be highly correlated with these gradients of changing precipitation, reflecting adaptive radiation along gradients of changing precipitation driven by reduced gene flow and differential patterns of directional selection. As we expected, variation in precipitation was a much stronger predictor of genetic differentiation than were other climatic variables or isolation by distance. The pattern of phylogenetic differentiation among Caragana species is also closely associated with gradients of changing patterns of precipitation, suggesting that differential precipitation plays a major role in driving the genetic differentiation and adaptive radiation of the Caragana genus in the region of the Ordos Plateau.


Caragana Landscape genetics Adaptive radiation Gene flow Climate gradients 



This work was supported by Science Foundation of Ministry of Science and Technology of China (2011BAC07B01).


  1. Amos J, Bennet AF, Mac Nally R, Newell G, Radford JQ, Pavlova A, Thompson J, White M, Sunnucks P (2012) Predicting landscape genetic consequences of habitat loss, fragmentation and mobility for species of woodland birds. Plos One 7:e30888PubMedCrossRefGoogle Scholar
  2. Bai J, Ge QS, Dai JH, Wang Y (2010) Relationship between woody plants phenology and climate factors in Xi’an, China. Chin J Plant Ecol 34(11):1274–1282Google Scholar
  3. Chang ZY, Zhang ML (1997) Anatomical structures of young stems and leaves of some Caragana species with their ecological adaptabilities. Bull Bot Res 17:66–71Google Scholar
  4. Chen XD, Dong XJ, Chen ZX (1999) Shrub diversity and its restoration ecology in Ordus Plateau Sandland. In: Ma KP (ed) Ecosystem diversity in key areas of China. Zhejiang Science and Technology Press, Hangzhou, pp 109–153Google Scholar
  5. Coyne JA, Orr AH (2004) Speciation. Sinauer Associates, SunderlandGoogle Scholar
  6. Cushman SA, Landguth EL (2010) Spurious correlations and inference in landscape genetics. Mol Ecol 19:3592–3602PubMedCrossRefGoogle Scholar
  7. Cushman SA, McKelvey KS, Hayden J, Schwartz MK (2006) Gene-flow in complex landscapes: testing multiple models with causal modeling. Am Nat 168:486–499PubMedCrossRefGoogle Scholar
  8. Cushman SA, Wasserman TN, Landguth EL, Shirk AJ (2013) Re-evaluating causal modeling with Mantel Tests in landscape genetics. Diverstiy 5:51–72. doi: 10.3390/d50x000x CrossRefGoogle Scholar
  9. de León LF, Bermingham E, Podos J, Hendry AP (2010) Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin’s finches. Philos Trans R Soc B 365:1041–1052CrossRefGoogle Scholar
  10. Doebeli M, Dieckmann U, Metz JA, Tautz D (2005) What we have also learned: adaptive speciation is theoretically plausible. Evolution 59:691–695PubMedGoogle Scholar
  11. Dong GY, Li BS, Gao SY (1983) The Quaternary ancient ecolian sands in the Ordos Plateau. Acta Geogr Sin 38(4):341–347Google Scholar
  12. Dormer EJ (1945) An investigation of the taxonomic value of shoot structure with special references of the Leguminosae. Ann Bot N S 9:141–161Google Scholar
  13. Doyle J (1999) DNA protocols for plants: CTAB total DNA isolation. In: Hewitt GM, Johnston A (eds) Molecular techniques in taxonomy. Springer, Berlin, pp 283–293Google Scholar
  14. Editorial Committee of Flora Reipublicae Popular Sinicae, Chinese Academy of Science (1993) Flora of China (42 vol part 1). Science Press, Beijing, pp 13–67Google Scholar
  15. Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259CrossRefGoogle Scholar
  16. Feder JL, Hunt TA, Bush L (1993) The effects of climate, host plant phenology and host fidelity on the genetics of apple and hawthorn infesting races of Rhagoletis pomonella. Entomol Exp Appl 69:117–135CrossRefGoogle Scholar
  17. Gavrilets S (2000) Waiting time to parapatric speciation. Proc R Soc B 570(267):2483–2492CrossRefGoogle Scholar
  18. Gavrilets S, Vose A (2007) Case studies and mathematical models of ecological speciation. 2. Palms on an oceanic island. Mol Ecol 16:2910–2921PubMedCrossRefGoogle Scholar
  19. Gavrilets S, Li H, Vose MD (2000) Patterns of parapatric speciation. Evolution 54(1126–559):1134Google Scholar
  20. Gorbunova NN (1984) De generis Caragana Lam. (Fabaceae) notae systematicae. Novosti Sist Vyssh Rast 21:92–100Google Scholar
  21. Grubov VI (1999) Plants of Central Asia, vol 1. Science Publishers, Inc., New HampshireGoogle Scholar
  22. Guillot G, Rousset F (2011) On the use of simple and partial Mantel tests in the presence of spatial auto-correlation. arXiv:1112.0651v1Google Scholar
  23. Guo ZX, Zhang XN, Wang ZM et al (2012) Responses of vegetation phenology in Northeast China to climate change. Chin J Ecol 29(3):578–585Google Scholar
  24. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high-resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  25. Hoelzer GA, Drewes R, Meier J, Doursat R (2008) Isolation-by-distance and outbreeding depression are sufficient to drive parapatric speciation in the absence of environmental influences. PLoS Comput Biol 4:e1000126PubMedCrossRefGoogle Scholar
  26. Iverson LR, Prasad AM (2002) Potential redistribution of tree species habitat under five climate change scenarios in the eastern US. For Ecol Manag 155:205–222CrossRefGoogle Scholar
  27. Komarov VL (1908) Generis Caragana monographia. Acta Hortic Petrop 29:77–388Google Scholar
  28. Komarov VL (1945) VL Komarov Opera Selecta. Academic Science Press URSS, Moscow, pp 159–342Google Scholar
  29. Kremer A, Ronce O, Robledo-Arnuncio JJ et al (2012) Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecol Lett 15:378–392CrossRefGoogle Scholar
  30. Kutzbach JE, Prell WL, Ruddiman WF (1993) Sensitivity of Eurasian Climate to surface up lift of the Tibetan Plateau. J Geol 101:177–190CrossRefGoogle Scholar
  31. Legendre P, Fortin M-J (2010) Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Mol Ecol 10:831–844CrossRefGoogle Scholar
  32. Li B (1990) Natural resources and environment research in Ordos Plateau, Inner Mongolia. Science Press, BeijingGoogle Scholar
  33. Li XR (1997) The characteristics of the flora of the shrub resource in Maowusu Sandland and the countermeasures for their protection. J Nat Res 12:146–152Google Scholar
  34. Li XR (2000) Discussion on the characteristics of shrubby diversity of Ordos Plateau. Resour Sci 22:54–59Google Scholar
  35. Liu XD, Li L, An ZS (2001) Tibetan Plateau uplift and drying in Eurasian interior and Northern Africa. Quat Sci 21(2):114–122Google Scholar
  36. Ma YQ (1989) Flora of Inner Mongolia, vol 3, 2nd edn. The Peoples Press of Inner Mongolia, HohhotGoogle Scholar
  37. Ma CC, Gao YB, Liu HF (2003) Interspecific transition among Caragana microphylla, C. davazamcii and C. korshinskii along geographic gradient. I. Ecological and RAPD evidence. Acta Bot Sin 45:1218–1227Google Scholar
  38. Manabe S, Broccoli AJ (1990) Mountains and arid climates of middle latitudes. Science Press, Beijing, pp 192–194Google Scholar
  39. Manabe S, Terpstra TB (1974) The effects of mountain s of the general circulation of the atmosphere by numerical experiments. J Atmos Sci 31:3–42CrossRefGoogle Scholar
  40. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  41. Mayr E (1954) Change of genetic environment and evolution. In: Huxley J, Hardy AC, Ford EB (eds) Evolution as a process. Allen & Unwin, London, pp 157–180Google Scholar
  42. McKinnon JS, Mori S, Blackman BK, David L, Kingsley DM et al (2004) Evidence for ecology’s role in speciation. Nature 429:294–298PubMedCrossRefGoogle Scholar
  43. Meirmans PG (2012) The trouble with isolation by distance. Mol Ecol 21:2839–2846PubMedCrossRefGoogle Scholar
  44. Nei M (1972) Genetic distance between populations. Am Nat 106:282–292CrossRefGoogle Scholar
  45. Niemiller ML, Fitzpatrick BM, Miller BT (2008) Recent divergence-with-gene-flow in Tenessee cave salamanders (Plethodontidae; Gyrinophylus) inferred from gene genealogies. Mol Ecol 17:2258–2275PubMedCrossRefGoogle Scholar
  46. Nix H (1986) A biogeographic analysis of Australian elapid snakes. Atlas of Elapid Snakes of Australia. Australian Government Publishing Service, CanberraGoogle Scholar
  47. Nosil P (2008) Speciation with gene flow could be common. Mol Ecol 17(2103–540):2106Google Scholar
  48. Rehfeldt GE, Crookston NL, Warwell MV, Evans JS (2006) Empirical analyses of plant-climate relationships for the western United States. Int J Plant Sci 167(6):1123–1150CrossRefGoogle Scholar
  49. Sanczir CZ (1979) Genus Caragana Lam. (systematic, geography, phylogeny and economic significance). In: Study on flora and vegetation of P. R. Mongolia, vol. 1. Academic Press, Ulan-Bator, pp 233–388Google Scholar
  50. Smouse PE, Long JC, Sokal RR (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632CrossRefGoogle Scholar
  51. Song CQ, You SC, Ke LH, Liu GH, Zhong XK (2012) Phenological variation of typical vegetation types in northern Tibet and its response to climate changes. Acta Ecol Sin 32(4):1045–1055CrossRefGoogle Scholar
  52. Wasserman TN, Cushman SA, Schwartz MK, Wallin DO (2010) Spatial scaling and multi-model inference in landscape genetics: Martes americana in northern Idaho. Landscape Ecol 25:1601–1612CrossRefGoogle Scholar
  53. Wiley EO (1991) The compleat cladist: a primer of phylogenetic procedures. Special publication no. 19. The University of Kansas Museum of Natural History, LawrenceGoogle Scholar
  54. Wright S (1932) The roles of mutation, inbreeding, cross breeding and selection in evolution, vol 1. In: Proceedings of the sixth international congress of genetics, pp 356–366 For more recent reviews of Wright’s theory, see S. Wright [Evolution 36,427 (1982)] and W. Provine [Sewall Wright and Evolutionary Biology (University of Chicago Press, Chicago, 1986)]Google Scholar
  55. Wu ZY (1980) Vegetation of China. Science Press, BeijingGoogle Scholar
  56. Yamamoto S, Sota T (2009) Incipient allochronic speciation by climatic disruption of the reproductive period. Proc R Soc B 276:2711–2719PubMedCrossRefGoogle Scholar
  57. Yang CY, Li N, Ma XQ (1990a) The floristic analysis of genus Caragana. Bull Bot Res 10(4):93–99Google Scholar
  58. Yang HY, Li N, Ma Q (1990b) The floristic analysis of genus Caragana. Bull Bot Res 10:93–99Google Scholar
  59. Yang JY, Yang J, Yang MB et al (2012) Genetic diversity of Caragana species of the Ordos Plateau in China. Plant Syst Evol 298:801–809CrossRefGoogle Scholar
  60. Ye DZ, Gao YX (1979) Meteorology of Qinghai-Xizang Plateau. Science Press, Beijing, pp 1–278Google Scholar
  61. Yeh FC, Yang RC, Boyle T (1999) POPGENE 32-version 1.31. Population Genetics Software.
  62. Yue LP, Li JX, Zheng GZ (2007) The Ordos Plateau evolution and environmental effect. Earth Sci 37:16–22Google Scholar
  63. Zhang ML (1997) A reconstructing phylogeny in Caragana (Fabaceae). Acta Bot Yunnan 19:331–341Google Scholar
  64. Zhang ML (1998) A preliminary analytic biogeography in Caragana (Fabaceae). Acta Bot Yunnan 20:1–11Google Scholar
  65. Zhang ML, Tian XY, Ning JC (1996) Pollen morphology and its taxonomic significance of Caragana Fabr. (Fabaceae) from China. Acta Phytotaxon Sin 34:397–409Google Scholar
  66. Zhang ML, Huang YM, Kang Y et al (2002) Floristics and vegetation of the genus Caragana in Ordos Plateau. Bull Bot Res 22:497–502Google Scholar
  67. Zhou DW (1996) Study on distribution of the genus caragana Fabr. Bull Bot Res 16(4):428–435Google Scholar
  68. Zhou DW, Wang AS, Li H (1994) Classification and distribution of Sect. Caragana, Caragana. J Northeast Norm Univ 2:64–68Google Scholar
  69. Zhou DW, Liu ZL, Ma YQ (2005) The study on phytogeographical distribution and differentiation of Caragana Fabr., Leguminosae. Bull Bot Res 25(04):471–487Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht (outside the USA) 2013

Authors and Affiliations

  • Jiuyan Yang
    • 1
  • Samuel A. Cushman
    • 2
  • Jie Yang
    • 1
  • Mingbo Yang
    • 1
  • Tiejun Bao
    • 1
  1. 1.School of Life SciencesInner Mongolia UniversityHohhotChina
  2. 2.USDA Forest Service/Rocky Mountain Research StationMissoulaUSA

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