Skip to main content
Log in

Allozyme Polymorphism of Swiss Stone Pine Pinus cembra L. in Mountain Populations of the Alps and the Eastern Carpathians

  • Plant Genetics
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Swiss stone pine Pinus cembra L. is a species with fragmented range, occurring in the Alpine-East Carpathian mountain system. Seeds of P. cembra are dispersed by nutcrackers, which offers potential possibilities for gene exchange among populations. Using isozyme analysis, we have examined five samples from two parts of the Swiss stone pine range: the Alps (Switzerland and Austria) and the Carpathians (two samples from the northern macroslope of the Gorgany Ridge, Eastern Carpathians, Ivano-Frankivs'ka oblast and one sample from Zakarpats'ka oblast of Ukraine). The allele frequencies of 30 isozyme loci, coding for enzymes ADH, FDH, FEST, GDH, GOT, IDH, LAP, MNR, MDH, PEPCA, 6-PGD, PGI, PGM, SDH, SKDH, SOD, were analyzed using cluster analysis and Principal Component Analysis. Two clusters, corresponding to the isolated Alpine and Carpathian parts of the range, were found. The main contribution to these differences were made by loci Adh-1, Adh-2, Fest-2, Lap-3, Mdh-4, and Sod-4. The interpopulation differentiation proved to be somewhat higher than that typical for pines (F ST = 7.4%), but within the limits characteristic for taxonomically close species. Thus, isolation of the populations did not lead to their marked differentiation, which may be explained by gene flow and balancing selection, which equalizes gene frequencies across the fragmented species area. Interlocus (F ST heterogeneity (from 0.003 to 0.173) suggests adaptive significance of some of the allozyme polymorphisms or linkage of some loci with adaptive genes. The Carpathian populations were shown to have higher gene diversity than the Alpine ones (expected heterozygosities 0.095–0.114 and 0.060–0.080, respectively). A deficiency of heterozygotes (as compared to the Hardy-Weinberg proportions), observed in the embryo sample, was probably explained by inbreeding. The reduction in the area of Carpathian pine forests in Holocene, caused by the global climatic changes and the anthropogenic impact, is hazardous for the gene pool of the species. The maintenance of genetic uniqueness of both Carpathian populations of P. cembra in general, and individual stands in particular, requires special measures for protection of Swiss stone pine in the Eastern Carpathians.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. Popov, M.G., Ocherk rastitel'nosti i flory Karpat (Essay on the Vegetation and Flora of the Carpathians), Moscow: MOIP, 1949.

    Google Scholar 

  2. Critchfield, W.B. and Little, E.L., Geographic Distribution of the Pines of the World, Washington, DC: US Dept. of Agric., 1966.

    Google Scholar 

  3. Bobrov, E.G., Lesoobrazuyushchie khvoinye SSSR (Forest-Forming Conifers of the Soviet Union), Moscow: Nauka, 1978.

    Google Scholar 

  4. Goncharenko, G.G., Padutov, V.E., and Silin, A.E., Population Structure, Gene Diversity and Differentiation in Natural Populations of Cedar Pines (Pinus subsect. cembrae, Pinaceae) in the USSR, Plant Syst. Evol., 1992, vol. 182, pp. 121–134.

    Article  CAS  Google Scholar 

  5. Gugerli, F., Senn, J., Anzidei, M., et al., Chloroplast Microsatellites and Mitochondrial nad1 Intron 2 Sequences Indicate Congruent Phylogenetic Relationships among Swiss Stone Pine (Pinus cembra), Siberian Stone Pine (Pinus sibirica), and Siberian Dwarf Pine (Pinus pumila), Mol. Ecol., 2001, vol. 10, no.6, pp. 1489–1497.

    Article  PubMed  CAS  Google Scholar 

  6. Goncharenko, G.G., Genosistematika i evolyutsionnaya filogeniya lesoobrazuyushchikh khvoinykh Palearktiki (Gene Systematics and Evolutionary Phylogeny of Forest-Forming Conifers of Palearctics), Minsk: Tekhnalogiya, 1999.

    Google Scholar 

  7. Goncharenko, G.G., Padutov, V.E., and Silin, A.E., Extent of Genetic Subdivision and Differentiation in Natural Populations of Cedar Pines, Dokl. Akad. Nauk SSSR, 1991, vol. 317, no.6, pp. 1477–1483.

    Google Scholar 

  8. Goncharenko, G.G. and Silin, A.E., Populyatsionnaya i evolyutsionnaya genetika sosen Vostochnoi Evropy i Sibiri (Population and Evolutionary Genetics of Pines from Eastern Europe and Siberia), Minsk: Tekhnalogiya, 1997.

    Google Scholar 

  9. Krutovsky, K.V. and Politov, D.V., Study of Interspecific and Intraspecific Differentiation of Eurasian Cedar Pines with the Use of Isozyme Loci and Miltidimensional Analysis, in Molekulyarnye mekhanizmy geneticheskikh protsessov (Molecular Mechanisms of Genetic Processes), Moscow: Nauka, 1992, pp. 87–96.

    Google Scholar 

  10. Krutovsky, K.V., Politov, D.V., and Altukhov, Yu.P., Interspecific Genetic Differentiation of Eurasian Cedar Pines by Isozyme Loci, Genetika (Moscow), 1990, vol. 26, no.4, pp. 694–707.

    Google Scholar 

  11. Politov, D.V., Allozyme Polymorphism, Genetic Differentiation and Mating System of Siberian Cedar Pine Pinus sibirica Du Tour, Cand. Sci. (Biol.) Dissertation, Moscow: Inst. Gen. Genet., 1989.

    Google Scholar 

  12. Shurkhal, A.V., Podogas, A.V., and Zhivotovsky, L.A., Phylogenetic Analysis of the Genus Pinus by Allozyme Loci: Genetic Differentiation of Subgenera, Genetika (Moscow), 1991, vol. 27, no.7, pp. 1193–1205.

    ISI  Google Scholar 

  13. Szmidt, A.E., Genetic Variation in Isolated Populations of Stone Pine (Pinus cembra), Silva Fennica, 1982, vol. 16, no.2, pp. 196–200.

    Google Scholar 

  14. Hamrick, J.L., The Distribution of Genetic Variation within and among Natural Plant Populations, Genet. Wild Population Management, 1983, pp. 335–348.

  15. Hamrick, J.L., Godt, M.J., and Sherman-Broyles, S., Factors Influencing Levels of Genetic Diversity in Woody Plant Species, New Forests, 1992, vol. 6, pp. 95–124.

    Article  Google Scholar 

  16. Hamrick, J.L. and Godt, M.J.W., Effects of Life History Traits on Genetic Diversity in Plant Species, Philos. Trans. R. Soc. L., 1996, vol. B351, pp. 1291–1298.

    Google Scholar 

  17. Belletti, P. and Gullace, S., Biodiversita'e struttura genetica in popolazioni di pino cembro e pino silvestre dell'arco alpino occidentale, Sherwood—Foreste ed Albergi Oggi, 1999, vol. 5, no.5, pp. 11–16.

    Google Scholar 

  18. Bergmann, F. and Hattemer, H.H., Isozyme Gene Loci and Their Alletic Variation in Pinus sylvestris L. and Pinus cembra L., Silvae Genet., 1995, vol. 44, nos. 5–6, pp. 286–289.

    Google Scholar 

  19. Politov, D.V. and Krutovskii, K.V., Allozyme Polymorphism, Heterozygosity, and Mating System of Stone Pines (Pinus, Subsection cembrae), Proc. Int. Workshop on Subalpine Stone Pines and Their Environment: The Status of Our Knowledge, Ogden, Utah: USDA Forest Service Intermountain Res. Station, 1994, pp. 36–42.

    Google Scholar 

  20. Shurkhal, A., Podogas, A., and Zhivotovsky, L., Allozyme Differentiation in the Genus Pinus, Silvae Genet., 1992, vol. 41, no.2, pp. 105–109.

    Google Scholar 

  21. Belokon, M.M., Politov, D.V., Belokon, Yu.S., et al., Genetic Differentiation of Pines of the Section Strobus: Data of Isozyme Analysis, Dokl. Akad. Nauk, 1998, vol. 358, no.5, pp. 699–702.

    CAS  Google Scholar 

  22. Pirko, Ya.V., Population Genetic Variation of Three Indigenous Pine Species of the Genus Pinus L. in the Ukrainian Carpathians and Roztochchi, Cand. Sci. (Biol.) Dissertation, Kiev: Inst. Klitinn. Biol. Gene Engineering, 2001.

    Google Scholar 

  23. Pirko, Ya.V., Genetic Variation of European Cedar Pine Pinus cembra L. in the Natural Population of the Ukrainian Carpathians, in Problemy fiziologii rastenii i genetiki na rubezhe tret'ego tysyacheletiya (Problems of Plant Physiology and Genetics on the Eve of the Third Millenium), Kiev: Inst. Fiziol. Rast. Genet., 2000, p. 105.

    Google Scholar 

  24. Podogas, A.V., Genetic Differentiation of the Genus Pinus by Allozyme Loci, Cand. Sci. (Biol.) Dissertation, Moscow: Inst. Gen. Genet., 1993.

    Google Scholar 

  25. Korshikov, I.I., Pirko, Ya.V., and Poberezhnik, I.I., Population Genetic Variation of Species of the Genus Pinus within and beyond the Carpathian National Natural Park, in National Natural Parks: Problems of Creation and Development, Yaremche, Ukraine: Ministry of Ecology and Natural Resources of Ukraine, Carpathian National Natural Park, 2000, pp. 164–167.

    Google Scholar 

  26. Tomback, D.F., Holtmeier, F.K., Mattes, H., et al., Tree Clusters and Growth Form Distribution in Pinus cembra, a Bird-Dispersed Pine, Arctic Alpine Res., 1993, vol. 25, no.4, pp. 374–381.

    Google Scholar 

  27. Clayton, J.W. and Tretiak, D.N., Amino-Citrate Buffers for pH Control in Starch Gel Electrophoresis, J. Fish. Res. Board Can., 1972, vol. 29, pp. 1169–1172.

    CAS  Google Scholar 

  28. Markert, C.L. and Faulhaber, I., Lactate Dehydrogenase Isozyme Patterns in Fish, J. Exp. Zool., 1965, vol. 159, no.2, pp. 319–332.

    PubMed  CAS  Google Scholar 

  29. Ridgeway, Y.J., Sherburne, S.W., and Lewis, R.D., Polymorphisms in the Esterases of Atlantic Herring, Trans. Am. Fish. Soc., 1970, vol. 99, pp. 147–151.

    Google Scholar 

  30. Swofford, D.L. and Selander, R.B., BIOSYS-1: A FORTRAN Program for the Comprehensive Analysis of Electrophoretic Data in Population Genetics and Systematics, J. Hered., 1981, vol. 72, pp. 281–283.

    Google Scholar 

  31. Yeh, F.C., Yang, R.C., and Boyle, T., PopGene Version 1.31: Microsoft Windows-Based Freeware for Population Genetic Analysis, 1998.

  32. Peakall, R. and Smouse, P.E., GenAIEx V5: Genetic Analysis in Excel, Population Genetic Software for Teaching and Research, Canberra, Australia: Austr. Nat. Univ., 2001; http://www.anu.edu.au/BoZo/GenAlEx/.

    Google Scholar 

  33. Wright, S., Evolution and the Genetics of Population, vol. 4: Variability within and among Natural Populations, Chicago: Univ. of Chicago Press, 1978.

    Google Scholar 

  34. Nei, M., Genetic Distance between Populations, Am. Nat., 1972, vol. 106, pp. 283–292.

    Article  Google Scholar 

  35. Nei, M., F-Statistics and Analysis of Gene Diversity in Subdivided Populations, Ann. Hum. Genet., 1977, vol. 41, pp. 225–233.

    PubMed  CAS  Google Scholar 

  36. Felsenstein, J., PHYLIP—Phylogeny Inference Package (Version 3.2), Cladistics, 1989, vol. 5, pp. 164–166.

    Google Scholar 

  37. STATISTICA for Windows (Computer Program Manual), Tulsa, OK: StatSoft, 1998.

  38. Krutovsky, K.V., Politov, D.V., and Altukhov, Yu.P., Genetic Variation of Siberian Cedar Pine Pinus sibirica Du Tour: I. Mechanisms of Genetic Control of Isozyme Systems, Genetika (Moscow), 1987, vol. 23, no.12, pp. 2216–2228.

    ISI  Google Scholar 

  39. Bergmann, F. and Gillet, E.M., Phylogenetic Relationships among Pinus Species (Pinaceae) Inferred from Different Numbers of 6PGDH Loci, Plant Syst. Evol., 1997, vol. 208, pp. 25–34.

    Article  Google Scholar 

  40. Lewandowski, A. and Burczyk, J., Mating System and Genetic Diversity in Natural Populations of European Larch (Larix decidua) and Stone Pine (Pinus cembra) Located at Higher Elevations, Silvae Genet., 2000, vol. 49, no.3, pp. 158–161.

    Google Scholar 

  41. Pirko, Ya.V. and Korshikov, I.I., Genetic Control of Isozymes in European Cedar Pine Pinus cembra L. of the Ukrainian Carpathians, Tsitol. Genet., 2001, no. 4, pp. 33–37.

  42. Politov, D.V., Belokon, M.M., Maluchenko, O.P., et al., Genetic Evidence of Natural Hybridization between Siberian Stone Pine, Pinus sibirica Du Tour, and Dwarf Siberian Pine, P. pumila (Pall.) Regel, Forest Genet., 1999, vol. 6, no.1, pp. 41–48.

    Google Scholar 

  43. Podogas, A.V., Shurkhal, A.V., Semerikov, V.L., and Rakitskaya, T.A., Genetic Variation of Needle Enzymes in Siberian Cedar Pine Pinus sibirica Du Tour, Genetika (Moscow), 1991, vol. 27, no.4, pp. 695–703.

    ISI  Google Scholar 

  44. Krutovsky, K.V. and Politov, D.V., Allozyme Polymorphism in a Natural Population of Siberian Pine Pinus sibirica Du Tour, in Problemy prikladnoi i populyatsionnoi genetiki (Problems of Applied and Population Genetics), Moscow, 1987, p. 142.

  45. Politov, D.V., Krutovsky, K.V., and Altukhov, Yu.P., Characterization of the Gene Pools of Cedar Pine Populations with a Set of Isozyme Loci, Genetika (Moscow), 1992, vol. 28, no.1, pp. 93–114.

    CAS  ISI  Google Scholar 

  46. Podogas, A.V., Shurkhal, A.V., Semerikov, V.L., and Zhivotovsky, L.A., Evaluation of Genetic Differentiation between Two Pine Species, Pinus sibirica subgenus strobus and P. sylvestris subgenus pinus with Samples from a Botanic Garden and Natural Populations, Genetika (Moscow), 1991, vol. 27, no.4, pp. 758–762.

    ISI  Google Scholar 

  47. Krutovskii, K.V., Politov, D.V., and Altukhov, Y.P., Isozyme Study of Population Genetic Structure, Mating System and Phylogenetic Relationships of the Five Stone Pine Species (Subsection Cembrae, Section Strobi, Subgenus Strobus), in Population Genetics and Genetic Conservation of Forest Trees, Amsterdam, the Netherlands: SPB Academic, 1995, pp. 279–304.

    Google Scholar 

  48. Politov, D.V. and Krutovskii, K.V., Phylogenetics, Genogeography and Hybridization of 5-Needle Pines in Russia and Neighboring Countries, Five-Needle Pine Species: Genetic Improvement, Disease Resistance, and Conservation: IUFRO Working Party, Proc. RMRS-P-32 (July 24–25, 2001, Medford, OR), Ogden, Utah: US Dept. of Agric., Forest Serv., Rocky Mountain Res. Station, 2004, pp. 38–50.

    Google Scholar 

  49. Belokon, M.M. and Politov, D.V., Evaluation of Genetic Diversity in Populations of Korean Cedar Pine Pinus koraiensis Sieb. et. Zucc., 1-ya molodezhnaya shkolakonferentsiya “Sokhranenie bioraznoobraziya prirodnykh resursov” (1st Conf. of Young Researchers “Preservation of Biodiversity of Natural Resources”), Moscow: Federal'naya Gosudarstvennaya Programma “Integratsiya,” 2000, p. 13.

    Google Scholar 

  50. Lanner, R.M., Biology, Taxonomy, Evolution and Geography of Stone Pines of the World, Proc. Symp. Whitebark Pine Ecosystems: Ecology and Management of a High-Mountain Resource, Ogden, Utah, 1990, pp. 14–24.

  51. Lanner, R.M., Made for Each Other: A Symbiosis of Birds and Pines, New York: Oxford Univ. Press, 1996.

    Google Scholar 

  52. Tomback, D., Nutcracker-Pine Mutualisms: Multi-Trunk Trees and Seed Size, Acta XIX Congr. Int. Ornithologici, Ottawa, O.N.: Univ. Press, 1988, pp. 518–527.

    Google Scholar 

  53. Tomback, D., Nutcrackers and Pines: Coevolution or Coadaptation?, Coevolution, Chicago, Univ. of Chicago Press, 1983, pp. 179–223.

    Google Scholar 

  54. Tomback, D. and Schuster, S., Genetic Population Structure and Growth Form Distribution in Bird-Dispersed Pines, Proc. Int. Workshop on Subalpine Stone Pines and Their Environment: The Status of Our Knowledge, Ogden, Utah: USDA Forest Service Intermountain Res. Station, 1994, pp. 43–50.

    Google Scholar 

  55. Tomback, D.F. and Linhart, Y.B., The Evolution of Bird-Dispersed Pines, Evol. Ecol., 1990, vol. 4, pp. 185–219.

    Article  Google Scholar 

  56. Mattes, H., Coevolutional Aspects of Stone Pines and Nutcrackers, Proc. Int. Workshop on Subalpine Stone Pines and Their Environment: The Status of Our Knowledge, Ogden, Utah: USDA Forest Service Intermountain Res. Station, 1994, pp. 31–35.

    Google Scholar 

  57. Rolando, A. and Carisio, L., Effects of Resource Availability and Distribution on Autumn Movements of the Nutcracker Nucifraga caryocatactes in the Alps, Proc. Int. Workshop on Subalpine Stone Pines and Their Environment: The Status of Our Knowledge, Ogden, Utah: USDA Forest Service Intermountain Res. Station, 1999, vol. 141, no.1, pp. 125–134.

    Google Scholar 

  58. Altukhov, Y.P., The Role of Balancing Selection and Overdominance in Maintaining Allozyme Polymorphism, Genetics, 1991, vol. 85, no.1, pp. 79–90.

    Google Scholar 

  59. Altukhov, Yu.P., Geneticheskie protsessy v populyatsiyakh (Genetic Processes in Populations), Moscow: Nauka, 2003.

    Google Scholar 

  60. Dinamika populyatsionnykh genofondov pri antropogennykh vozdeistviyakh (Dynamics of Population Gene Pools under Anthropogenic Influences), Altukhov, Yu.P., Ed., Moscow: Nauka, 2004.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

__________

Translated from Genetika, Vol. 41, No. 11, 2005, pp. 1538–1551.

Original Russian Text Copyright © 2005 by M. Belokon, Yu. Belokon, Politov, Altukhov.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Belokon, M.M., Belokon, Y.S., Politov, D.V. et al. Allozyme Polymorphism of Swiss Stone Pine Pinus cembra L. in Mountain Populations of the Alps and the Eastern Carpathians. Russ J Genet 41, 1268–1280 (2005). https://doi.org/10.1007/s11177-005-0228-0

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11177-005-0228-0

Keywords

Navigation