Abstract
In recent years, land use changes led to a rapid decline and fragmentation of J. communis populations in Germany. Population isolation may lead to a restricted gene flow and, further, to negative effects on genetic variation. In this study, genetic diversity and population structure in seven fragmented J. communis populations in Saxony, Germany, were investigated using nuclear microsatellites (nSSR) and chloroplast single nucleotide polymorphism (cpSNP). In all Saxony J. communis populations, a high genetic diversity was determined but no population differentiation could be detected whatever method was applied (Bayesian cluster analysis, F-statistics, AMOVA). The same was true for three J. communis out-group samples originating from Italy, Slovakia and Norway, which also showed high genetic diversity and low genetic differences regarding other J. communis populations. Low genetic differentiation among the J. communis populations ascertained with nuclear and chloroplast markers indicated high levels of gene flow by pollen and also by seeds between the sampled locations. Low genetic differentiation may also provide an indicator of Juniper survival during the last glacial maximum (LGM) in Europe. The results of this study serve as a basis for the implementation of appropriate conservation measures in Saxony.
References
Alb aladejo R., Guzman B., Gonzalez-Martinez S. & Aparicio A. 2012. Extensive pollen flow but few pollen donors and high reproductive variance in an extremely fragmented landscape. PLoS ONE 7(11): e49012.
Ashley M. 2010. Plant Parentage, Pollination, and Dispersal: How DNA Microsatellites have altered the landscape. Crc. Cr. Rev. Plant. Sci. 29: 148-161.
Bai W., Wang W. & Zhang D. 2014. Contrasts between the phylogeographic patterns of chloroplast and nuclear DNA highlight a role for pollen-mediated gene flow in preventing population divergence in an East Asian temperate tree. Mol. Phylogenet. Evol. 81: 37-48.
Berube Y., Ritland C. & Ritland K. 2003. Isolation, characterization, and cross-species utility of microsatellites in yellow cedar (Chamaecyparis nootkatensis). Genome NRC 46(3): 353-61.
Bettencourt S. X., Mendonça D., Lopes M. S., Rocha S., Monjardino P., Monteiro L. & da Câmara Machado A. 2015. Genetic diversity and population structure of the endemic Azorean juniper, Juniperus brevifolia (Seub.) Antoine, inferred from SSRs and ISSR markers. Biochem. Syst. Ecol. 59: 314-324
Bezault E., Rognon X., Gharbi K., Baroill er J. F., & Bernard Chevassus B. 2012. Microsatellites cross-species amplification across some African Cichlids. Int J Evol Biol. doi.org/10.1155/2012/870935
Broome A. 2003. Growing Juniper: Propagation and establishment practices. Forestry Commission 50: 1-12.
Burczyk J. & Chybicki I. J. 2004. Cautions on direct gene flow estimation in plant populations. Evolution. I.E.V.J. 58 (5): 956-63.
Chase M. W. & Hill s H. H. 1991. Silica-Gel - An ideal material for field preservation of leaf samples for DNA Studies. Taxon 40(2): 215-220.
Couvet D. 2002. Deleterious effects of restricted gene flow in fragmented populations. Conserv. Biol. 16: 369-376.
Diekmann K. Hodkinson T. R. & Barth S. 2012. New chloroplast microsatellite markers suitable for assessing genetic diversity of Lolium perenne and other related grass species. Ann. Bot. 110(6): 1327-39.
Earl D. & von Holdt B. 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Gen. Res. 4(2): 359-361.
Ellenberg H. 1996. Vegetation Mitteleuropas mit den Alpen in ökologischer, dynamischer und historischer Sicht. 5. Auflage. 1095 pp. Verlag UTB, Stuttgart.
Ennos R. 1994. Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72: 250-259.
Evanno G., Regnaut S. & Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14(8): 2611-20.
Feng Y. H., Yang Z. Q., Wang J., Luo Q. F. & Li H. G. 2014. Development and characterization of SSR markers from Pinus massoniana and their transferability to P. elliottii, P. caribaea and P. yunnanensis. Gen. Mol. Res., GMR 13(1): 1508-13.
Ferreira M. & Eriksson G. 2006. A programme for the management of forest three genetic resources in the Azores islands. Silva Lus. 14(1): 59-73.
Furnier G. & Stine M. 1995. Interpopulation differentiation of nuclear and chloroplast loci in white spruce. Can. J. For. Res. 25(5): 736-742.
Govindaraju D. R. 1989. Estimates of gene flow in forest trees. Biol. J. Linn. Soc. 37(4): 345-357.
Gruwez R., Leroux O., De Frenne P., Tack W., Viane R. & Verheyen K. 2012. Critical phases in the seed development of common juniper (Juniperus communis). Plant. Biol. 5(1): 210-219.
Hamrick J. 2004. Response of forest trees to global environmental changes. For. Ecol. Manage. 197: 323-335.
Hendrix R., Hauswaldt J., Veith M. & Steinfartz S. 2010. Strong correlation between cross-amplification success and genetic distance across all members of ‘True Salamanders’ (Amphibia: Salamandridae) revealed by Salamandra salamandra-specific microsatellite loci. Mol. Ecol. Resour. 10(6):1038-47.
Keir K. R., Bemmels J. B. & Aitken S. N. 2011. Low genetic diversity, moderate local adaptation, and phylogeographic insights in Cornus nuttallii (Cornaceae). Am. J. Bot. 98(8): 1327-36.
Khantemirova E. V. & Semerikov V. L. 2010. Genetic variation of some varieties of common juniper Juniperus communis L. inferred from analysis of allozyme loci. Genetika 46(5): 622-30.
Leonardi S., Piovani P., Scalf i M., Piotti A., Logiannini R. & Menozz i P. 2012: Effect of habitat fragmentation on the genetic diversity and structure of peripheral populations of beech in Central Italy. J. Heredity. 103(3): 408-417
Lu S. Y., Peng C. I., Cheng Y. P., Hong K. H. & Chiang T. Y. 2001. Chloroplast DNA phylogeography of Cunninghamia konishii (Cupressaceae), an endemic conifer of Taiwan. Genome N.R.C Canada 44(5): 797-807.
Marín J.C., Orozco-ter Wengel P., Romero K., Vásquez J.P., Varas V. & Vianna J.A. 2014. Cross-amplification of nonspecific microsatellites markers: a useful tool to study endangered/vulnerable species of southern Andes deer. Genet Mol Res 13: 3193-3200
McCartan S. & Gosling P. 2013. Guidelines for seed collection and stratification of Common Juniper (Juniperus communis L.). Tree Plant. Note 56(1): 24-29.
Michalczyk I. 2008. Application of DNA marker systems to test for genetic imprints of habitat fragmentation in Juniperus communis L. on different spatial and temporal scales. Dissertation, University Marburg, http://archiv.ub.uni-marburg.de/diss/z2008/0912
Michalczyk I., Lücke Y., Huck S. & Ziegenhagen B. 2010. Genetic support for perglacial survival of Juniperus communis L. in Central Europe. Holocene 20(6): 887-894.
Michalczyk I., Sebastiani F., Buonamici A., Cremer E., Mengel C., Ziegenhagen B. & Vendramin G. 2006. Characterization of highly polymorphic nuclear microsatellite loci in Juniperus communis L. Mol. Ecol. Notes 6(6): 346-348.
Nei M. (1973) Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. USA. 70: 3321-3323.
Neigel J. 2002. Is FST obsolete? Conserv. Gen. 3: 167-173.
Oostermeijer J. & De Knegt B. 2004. Genetic population structure of the wind-pollinated, dioecious shrub Juniperus communis in fragmented Dutch heathlands. Plant. Species. Biol. 19: 175-184.
Opgenoorth L. 2009. Identification and characterization of microsatellite marker in the tetraploid Juniperus tibetica Kom. using next generation sequencing. Conserv. Gen. Res. 1: 253-255.
Parchman T., Benkman C., Jenkins B. & Buerkle C. 2011. Low levels of population genetic structure in Pinus contorta (Pinaceae) across a geographic mosaic of co-evolution. Am. J. Bot. 98: 669-679.
Peakall R. & Smouse P. E. 2012. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research - an update. Bioinformatics Oxford, England 28(19): 2537-9.
Pépin L., Amigues Y., Lépingl e A., Berthier J. L., Bensaid A. & Vaiman D. 1995. Sequence conservation of microsatellites between Bos taurus (cattle), Capra hircus (goat) and related species. Examples of use in parentage testing and phylogeny analysis. Heredity 74(1): 53-61.
Petit R., Duminil J., Fineschi S., Hampt A., Salv ini D. & Vendramin G. 2005. Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Mol. Ecol. 14: 689-701.
Porth I. & El-Kassaby Y. A. 2014. Assessment of the genetic diversity in forest tree populations using molecular markers. Diversity 6: 283-295.
Pritchard J., Stephens M. & Donnell y P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
Provan J., Beatty G. E., Hunter A. M., McDonald R. A., McLaughlin E., Preston S. J. & Wilson S. 2009. Restricted gene flow in fragmented populations of a wind-pollinated tree. Conserv. Gen. 9: 1521-1532.
Provan J., Soranzo N., Wilson N., McNicol J. W., Forrest G., Cottrell J. & Powell W. 1998. Gene-pool variation in Caledonian and European Scots pine (Pinus sylvestris L.) revealed by chloroplast simple-sequence repeats. Proc. Biol. Sci. 265 (1407): 1697-705.
Reim S., Höltken A. & Höfer M. 2012. Diversity of the European indigenous wild apple (Malus sylvestris (L.) Mill.) in the East Ore Mountains (Osterzgebirge), Germany: II. Genetic characterization. Gen. Res. Crop. Evol. 60(3): 879-892
Ribeiro M., Mariette M. S., Vendramin G. G., Szmidt A. E., Plomion C. & Kremer A. 2002. Comparison of genetic diversity estimates within and among populations of maritime pine using chloroplast simple-sequence repeat and amplified fragment length polymorphism data. Mol. Ecol. 11(5): 869-77.
Robertson A., Newton A. & Ennos R. 2004. Multiple hybrid origins, genetic diversity and population genetic structure of two endemic Sorbus taxa on the Isle of Arran, Scotland. Mol. Ecol. 13(1): 123-34.
Robledo-Arnuncio J. & Gil L. 2005. Patterns of pollen dispersal in a small population of Pinus sylvestris L. revealed by total-exclusion paternity analysis. Heredity 94(1): 13-22.
Scheepens J. F., Frei E. S. & Stocklin J. 2013. Glacial history affected phenotypic differentiation in the alpine plant, Campanula thyrsoides. PLoS ONE 8(10): e73854.
Severns P. 2003. Inbreeding and small population size reduce seed set in a threatened and fragmented plant species, Lupinus sulphureus ssp. kincaidii (Fabaceae). Biol. Conserv.110: 221-229.
Slatkin M. 1987. Gene flow and the geographical structure of natural populations. Science 236(4803): 787-792. http://dx.doi.org/10.1126/science.3576198.
Soleimani V., Baum B. & Johnson D. 2003. Efficient validation of single nucleotide polymorphisms in plants by allele-specific PCR, with an example from barley. Plant Mol. Biol. Report. 21: 281-288.
Terrab A., Paun O., Talavera S., Tremetsberger K., Arista M. & Stuessy T. F. 2006. Genetic diversity and population structure in natural populations of Moroccan Atlas cedar (Cedrus atlantica; Pinaceae) determined with cpSSR markers. Am. J. Bot. 93(9): 1274-80.
Thomas P., El-barghati M. & Polwart A. 2007. Biological Flora of the British Isles: Juniperus communis L. J. Ecol. 95(6): 1404-1440.
Van der Merwe M., Winfield M. O., Arnold G. M. & Parker J. S. 2000. Spatial and temporal aspects of the genetic structure of Juniperus communis populations. Mol. Ecol. 9: 379-386.
Vanden-Broeck A., Gruwez R., Cox K., Adriaenssens S., Michalczyk I. & Verheyen K. 2011. Genetic structure and seed-mediated dispersal rates of an endangered shrub in a fragmented landscape: a case study for Juniperus communis in northwestern Europe. BMC Genetics 12(73).
Vinyallonga, S. L., Alv arado, J. L., Constantinidis, T., de la Serna, A. S., & García-Jacas, N. 2011. Microsatellite cross-species amplification in the genus Centaurea (Compositae). Collectanea Botánica 30: 17-27.
Vranckx G., Jacquemyn H., Muys B. & Honnay O. 2012. Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conserv. Biol. 26(2):228-37.
Whitlock M. C. & McCauley D. E. 1999. Indirect measures of gene flow and migration: FST not equal to 1/(4Nm + 1). Heredity 82: 117-125.
Wright S. 1978. Evolution and the Genetics of Population, Variability Within and Among Natural Populations. 590 pp. The University of Chicago Press, Chicago.
Young A., Boyle T. & Brown T. 1996. The population genetic consequences of habitat fragmentation for plants. Trends. Ecol. Evol. 11(10): 413-418.
Zhang Q., Chiang T., George M., Liu J. & Abb ott R. 2005. Phylogeography of the Qinghai-Tibetan Plateau endemic Juniperus przewalskii (Cupressaceae) inferred from chloroplast DNA sequence variation. Mol. Ecol. 14(11): 3513-24.
Zhang Q., Yan-Zhuo Y., Wu G., Zhang D. & Liu J. 2008. Isolation and characterization of microsatellite DNA primers in Juniperus przewalskii Kom (Cupressaceae). Conserv. Gen. 9: 767-769.