Abstract
Geological events and glacial history have all induced habitat fragmentation, which has long been recognized as a major threat to the survival of many species. However, fragmentation has differential effects on population genetic patterns of individual species, such as loss of genetic diversity, genetic differentiation enhance, inbreeding increase, allelic deletion, and no effect. Calocedrus macrolepis Kurz is an endangered ancient relictual and fragmented conifer. In this study, the genetic diversity and structure were analyzed to shed light on the factors that determine their contemporary genetic patterns and to provide optimum strategies for future conservation. The genetic diversity within and among 14 extant populations of C. macrolepis was analyzed using nine microsatellite markers. The genetic diversity (H E = 0.636), genetic differentiation (F ST = 0.163), and gene flow (Nm = 1.496) were disclosed, respectively. No significant correlation was detected by the Mantel test between genetic and geographical distances among pair-wise comparisons of populations (r = 0.197, P = 0.103). Fourteen populations could be generally assigned to two separate groups, and significant asymmetrical migration among populations within the regional groups was revealed. Both Quaternary glaciations and neotectonic movements seem to be associated with a long history of population contraction and fragmentation of C. macrolepis, enhancing its genetic drift and population divergence. The results indicate that long-term habitat fragmentation could be responsible for the genetic structure observed. In situ conservation strategies should be designed, especially small and isolated populations. Also, special attention should be given to populations LY and DZ because of their private alleles, as well as to population CJ isolated from the mainland.
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Acheré V, Favre JM, Besnard G, Jeandroz S (2005) Genomic organization of molecular differentiation in Norway spruce (Picea abies). Mol Ecol 14:3191–3201
Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188
Alistair SJ, Josep P (2006) Genetic effects of chronic habitat fragmentation in a wind-pollinated tree. P Natl Acad Sci USA 103:8096–8100
Allnutt TR, Newton AC, Lara A, Premoli A, Armesto JJ, Vergara R, Gardner M (1999) Genetic variation in Fitzroya cupressoides (alerce), a threatened South American conifer. Mol Ecol 8:975–987
Averyanov LV, Hiep NT, Loc PK (2008) The Genus Calocedrus (Cupressaceae) in the Flora of Vietnam. Taiwania 53:11–22
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge
Avise JC, Hamrick JL (1996) Conservation genetics: case histories from nature. Chapman & Hall, New York
Bacles CFE, Lowe AJ, Ennos RA (2004) Genetic effects of chronic habitat fragmentation on tree species: the case of Sorbus aucuparia in a deforested Scottish landscape. Mol Ecol 13:573–584
Bacles CFE, Burczyk J, Lowe AJ, Ennos RA (2005) Historical and contemporary mating patterns in remnant populations of the forest tree Fraxinus excelsior L. Evolution 59:979–990
Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165
Bekessy SA, Allnutt TR, Premoli AC, Lara A, Ennos RA, Burgman MA, Cortes M, Newton AC (2002) Genetic variation in the vulnerable and endemic Monkey Puzzle tree, detected using RAPDs. Heredity 88:243–249
Boratyński A, Wachowiak W, Dering M, Boratyńska K, Sękiewicz K, Sobierajska K, Jasińska AK, Klimko M, Montserrat JM, Romo A, Ok T, Didukh Y (2014) The biogeography and genetic relationship of J. oxycedrus and related taxa from the Mediterranean and Macaronesian regions. Bot J Linn Soc 174:637–653
Chen CH, Huang JP, Tsai CC, Chaw SM (2009) Phylogeny of Calocedrus (Cupressaceae), an eastern Asian and western North American disjunct gymnosperm genus, inferred from nuclear ribosomal nrITS sequences. Bot Stud 50:425–433
Craft KJ, Ashley MV, Koenig WD (2002) Limited hybridization between Quercus lobata and Quercus douglasii (Fagaceae) in a mixed stand in central coastal California. Am J Bot 89:1792–1798
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem bull 19:11–15
Ellstrand NC (1992) Gene flow by pollen: implications for plant conservation genetics. Oikos 63:77–86
Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Fahrig L, Merriam G (1994) Conservation of fragmented populations. Conserv Biol 8:50–59
Farjon A (2001) World checklist and bibliography of conifers. The Royal Botanic Gardens Press, Kew
Farjon A (2005) A monograph of Cupressaceae and Sciadopitys. The Royal Botanic Gardens Press, Kew
Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
Fu LG (1995) China plant red data book. Science Press, Beijing
Fu LG, Yu YF (1999) Cupressaceae. In: Raven PH, Wu CY (eds) Flora of China. Science Press, Missouri Botanical Garden Press, Beijing, St. Louis
Galeuchet DJ, Perret C, Fischer M (2005) Microsatellite variation and structure of 28 populations of the common wetland plant, Lychnis floscuculi L., in a fragmented landscape. Mol Ecol 14:991–1000
Ge S, Hong D, Wang H, Liu Z, Zhang C (1998) Population genetic structure and conservation of an endangered conifer, Cathaya argyrophylla (Pinaceae). Int J Plant Sci 159:351–357
GENEPOP (2013) Genepop - population genetics software. http://genepop.curtin.edu.au/
González-Martínez SC, Dubreuil M, Riba M, Vendramin GG, Sebastiani F, Mayol M (2010) Spatial genetic structure of Taxus baccata L. in the western Mediterranean Basin: past and present limits to gene movement over a broad geographic scale. Mol Phylogenet Evol 55:805–815
Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New Forest 6:95–124
Hanski I, Ovaskainen O (2002) Extinction debt at extinction threshold. Conserv Biol 16:666–673
Honnay O, Jacquemyn H, Bossuyt B, Hermy M (2005) Forest fragmentation effects on patch occupancy and population viability of herbaceous plant species. New Phytol 166:723–736
Hsieh YC, Chung JD, Wang CN, Chang CT, Chen CY, Hwang SY (2013) Historical connectivity, contemporary isolation and local adaptation in a widespread but discontinuously distributed species endemic to Taiwan, Rhododendron oldhamii (Ericaceae). Heredity 111:147–156
Khasa DP, Jaramillo-Correa JP, Jaquish B, Bousquet J (2006) Contrasting microsatellite variation between subalpine and western larch, two closely related species with different distribution patterns. Mol Ecol 15:3907–3918
Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. P Natl Acad Sci USA 75:2868–2872
Kracek Z (1999) An ancient Calocedrus (Cupressaceae) from the European Tertiary. Flora: Morphol Geobot, Oekophysiol 194:237–248
Kwak MM, Velterop O, van Andel J (1998) Pollen and gene flow in fragmented habitats. Appl Veg Sci 1:37–54
Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460
Ledig FT, Capó-Arteaga MA, Hodgskiss PD, Sbay H, Flores-López C, Thompson Conkle M, Bermejo-Velázquez B (2001) Genetic diversity and the mating system of a rare Mexican piñon, Pinus pinceana, and a comparison with Pinus maximartinezii (Pinaceae). Am J Bot 88:1977–1987
Liao SX, Mi XJ, Liu AZ, Kun L, Yang ZY (2010) Isolation and characterization of polymorphic microsatellite markers in Calocedrus macrolepis Kurz (Cupressaceae). HortScience 45:169–171
Liao SX, Cui K, Wan YM, Zhou ZS, Li ZH, Cui YZ (2014) Reproductive biology of the endangered cypress Calocedrus macrolepis. Nord J Bot 32:98–105
Lindborg R, Eriksson O (2004) Historical landscape connectivity affects present plant species diversity. Ecology 85:1840–1845
Liu YS, Guo SX, Ferguson DK (1996) Catalogue of cenozoic megafossil plants in China. Palaeontogr Abt B 238:141–179
Liu FY, Li K, Liao SX, Cui YZ (2010) Interspecific competition, population structure and growth dynamics of endangered Calocedrus macrolepis. Sci Silvae Sin 46:23–28
Lowe AJ, Boshier D, Ward M, Bacles CFE, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95:255–273
Maghuly F, Pinsker W, Praznik W, Fluch S (2006) Genetic diversity in managed subpopulations of Norway spruce [Picea abies (L.) Karst.]. Forest Ecol Manag 222:266–271
Mariette S, Chagne D, Lezier C, Pastuszka P, Raffin A, Plomion C, Kremer A (2001) Genetic diversity within and among Pinus pinaster populations: comparison between AFLP and microsatellite markers. Heredity 86:469–479
Matusova R (1995) Genetic variation in five populations of silver fir (Abies alba Mill.) in Slovakia. Biologia 50:53–59
Mehes M, Nkongolo KK, Michael P (2009) Assessing genetic diversity and structure of fragmented populations of eastern white pine (Pinus strobus) and western white pine (P. monticola) for conservation management. J Plant Ecol 2:143–151
MIGRATE-N 3.6.5 (2013) Estimation of population sizes and gene flow using the coalescent Software. Current version 3.6.5. http://popgen.sc.fsu.edu/Migrate-n.html
Miller MP (1997) Tools for population genetic analysis (TFPGA), version 1.3: a windows program for the analysis of allozyme and molecular population genetics data. http://www.markgeneticsoftware.net/
Milligan BG, Leebens-Mack J, Strand AE (1994) Conservation genetics: beyond the maintenance of marker diversity. Mol Ecol 3:423–435
Mona S, Ray N, Arenas M, Excoffier L (2014) Genetic consequences of habitat fragmentation during a range expansion. Heredity 112:291–299
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 512:354–362
Newman D, Tallmon DA (2001) Experimental evidence for beneficial fitness effects of gene flow in recently isolated populations. Conserv Biol 15:1054–1063
Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155
Oostermeijer J, Van’t Veer R, Den Nijs J (1994) Population structure of the rare, long-lived perennial Gentiana pneumonanthe in relation to vegetation and management in the Netherlands. J Appl Ecol 31:428–438
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214
Premoli AC, Kitzberger T, Veblen TT (2000) Isozyme variation and recent biogeographical history of the long-lived conifer Fitzroya cupressoides. J Biogeogr 27:251–260
Premoli AC, Souto CP, Allnut TR, Newton AC (2001) Effects of population disjunction on isozyme variation in the widespread Pilgerodendron uviferum. Heredity 87:337–343
Premoli AC, Souto CP, Rovere AE, Allnut TR, Newton AC (2002) Patterns of isozyme variation as indicators of biogeographic history in Pilgerodendron uviferum (D. Don) Florín. Divers Distrib 8:57–66
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Quiroga MP, Premoli AC (2010) Genetic structure of Podocarpus nubigena (Podocarpaceae) provides evidence of Quaternary and ancient historical events. Palaeogeogr Palaeoclimatol 285:186–193
Rallo P, Dorado G, Martín A (2000) Development of simple sequence repeats (SSRs) in olive tree (Olea europaea L.). Theor Appl Genet 101:984–989
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Rohlf FJ (1997) NTSYS-pc: numerical taxonomy and multivariate analysis system. Version 2.11c. Exeter Software, Setauket
Rumball W, Franklin IR, Franklin R, Sheldon BL (1994) Decline in heterozygosity under full-sib and double first-cousin inbreeding in Drosophia melanogaster. Genetics 136:1039–1049
Rumeu B, Vargas P, Jaén-molina R, Nogales M, Caujapé-castells J (2014) Phylogeography and genetic structure of the threatened Canarian Juniperus cedrus (cupressaceae). Bot J Linn Soc 175:376–394
Savolainen O, Pyhäjärvi T (2007) Genomic diversity in forest trees. Curr Opin Plant Biol 10:162–167
Schaal B, Hayworth D, Olsen K, Rauscher J, Smith W (1998) Phylogeographic studies in plants: problems and prospects. Mol Ecol 7:465–474
Sefc K, Lopes M, Mendonça D, Santos MRD, Machado L, Machado ADC (2000) Identification of microsatellite loci in olive(Olea europaea) and their characterization in Italian and Iberian olive trees. Mol Ecol 9:1171–1173
Sork VL, Nason J, Campbell DR, Fernandez JF (1999) Landscape approaches to historical and contemporary gene flow in plants. Trends Ecol Evol 14:219–223
Tang S, Dai W, Li M, Zhang Y, Geng Y, Wang L, Zhong Y (2008) Genetic diversity of relictual and endangered plant Abies ziyuanensis (Pinaceae) revealed by AFLP and SSR markers. Genetica 133:21–30
Tomimatsu H, Ohara M (2003) Genetic diversity and local population structure of fragmented populations of Trillium camschatcense (Trilliaceae). Biol Conserv 109:249–258
Torres-Díaz C, Ruiz E, González F, Fuentes G, Cavieres LA (2007) Genetic diversity in Nothofagus alessandrii (Fagaceae), an endangered endemic tree species of the Coastal Maulino Forest of Central Chile. Ann Bot 100:75–82
Van Geert A, Van Rossum F, Triest L (2008) Genetic diversity in adult and seedling populations of Primula vulgaris in a fragmented agricultural landscape. Conserv Genet 9:845–853
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Wang X, Zou Y, Zhang D, Hong D (1996) RAPD analysis of genetic diversity of Cathaya argyrophylla. Sci China (Serial C) 26:54–59
Wang DL, Li ZC, Hao G, Chiang TY, Ge XJ (2004) Genetic diversity of Calocedrus macrolepis (Cupressaceae) in southwestern China. Biochem Syst Ecol 32:797–807
WCMC (1997) The Socialist Republic of Vietnam Appendix 5-threatened plant species. http://www.wcmc.org.uk/infoserv/countryp/vietnam/app5.html
WGCPC (The Writing Group of Cenozoic Plants of China) (1978) Cenozoic plants from China. In: WGCPC (ed) Fossil plants of China. Science Press, Beijing, p 15
Yao X, Ye Q, Kang M, Huang H (2007) Microsatellites analysis reveals interpopulation differentiation and gene flow in endangered tree Changiostyrax dolichocarpa (Styracaceae) with fragmented distribution in central China. New Phytol 176:472–480
Yeh FC, Yang RC, Boyle T, Ye ZH, Mao JX (1997) POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418
Acknowledgments
The authors would like to thank Mr. Priscilla Anne Licht for his help in language editing of the manuscript, and Hongtao Li, Longqian Xiao and Rong Huang for their assistance and advice.
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This work was supported by the Forestry Science and Technology Extension Project (Grant Number 2015[35]), the Forest Commonweal Foundation of Chinese State Forestry Administration (Grant Number 200704029) and the Knowledge Innovation Program of the Chinese Academy of Sciences (Grant Number KSCX2-YW-G-035-1).
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Shengxi Liao and Kai Cui have contributed equally to this work.
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Liao, S., Cui, K., Tian, B. et al. The effect of long-term historical habitat fragmentation on genetic diversity of the relictual conifer Calocedrus macrolepis (Cupressaceae) in China. Braz. J. Bot 38, 567–577 (2015). https://doi.org/10.1007/s40415-015-0168-4
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DOI: https://doi.org/10.1007/s40415-015-0168-4