1. bookVolume 61 (2012): Issue 1-6 (December 2012)
Journal Details
First Published
22 Feb 2016
Publication timeframe
1 time per year
access type Open Access

Gene exchange across a postglacial contact zone in Fraxinus excelsior L.

Published Online: 01 Aug 2017
Page range: 18 - 27
Received: 09 Mar 2011
Journal Details
First Published
22 Feb 2016
Publication timeframe
1 time per year

Hybridization between divergent lineages of common ash Fraxinus excelsior L. was studied in Slovakia and adjacent regions of Hungary, the Czech Republic and Poland in the contact zone between two postglacial colonization routes originating from different glacial refugia. Thirty-eight common ash populations were studied using a combination of 6 maternally inherited chloroplast microsatellite markers and 7 biparentally inherited nuclear microsatellites (nSSR). Two predominant chloroplast lineages were identified, between which the boundary was very sharp. Populations containing a mixture of different haplotypes were found only in the immediate proximity of the boundary. Bayesian analysis of population structure based on nSSR loci revealed the existence of two clusters, which largely coincided with chloroplast lineages. Both haplotype frequencies and proportions of clusters identified by the Bayesian analysis exhibited a clinal transition over the hybrid zone, with cline widths of 36 km for chloroplast haplotype frequencies (reflecting gene flow by seeds) and 275 km for Bayesian clusters based on nSSR (reflecting gene flow by pollen and seeds). Chloroplast haplotype diversity increased along the boundary between lineages not only because of admixture, but also due to the presence of rare haplotypes. In contrast, diversity at nuclear loci did not exhibit any geographical trend.


BACLES, C. F. E., J. BURCZYK, A. J. LOWE and R. A. ENNOS (2005): Historical and contemporary mating patterns in remnant populations of the forest tree Fraxinus excelsior L. Evolution 59: 979-990.10.1554/04-653Search in Google Scholar

BACLES, C. F. E. and R. A. ENNOS (2008): Paternity analysis of pollen-mediated gene flow for Fraxinus excelsior L. in a chronically fragmented landscape. Heredity 101: 368-380.10.1038/hdy.2008.6618648389Search in Google Scholar

BARTON, N. H. and G. M. HEWITT (1985): Analysis of hybrid zones. Ann. Rev. Ecol. Syst. 16: 113-148.Search in Google Scholar

BIRCHLER, J. A., H. YAO and S. CHUDALAYANDI (2006): Unraveling the genetic basis of hybrid vigor. Proc. Natl. Acad. Sci. USA 103: 12957-12958.10.1073/pnas.0605627103155973216938847Search in Google Scholar

BLEEKE, W., U. SCHMITZ and M. RISTOW (2007): Interspecific hybridisation between alien and native plant species in Germany and its consequences for native biodiversity. Biol. Cons. 137: 248-253.10.1016/j.biocon.2007.02.004Search in Google Scholar

BRACHET, S., M. F. JUBIER, M. RICHARD, B. JUNG-MULLER and N. FRASCARIA-LACOSTE (1999): Rapid identification of microsatellite loci using 5 anchored PCR in the common ash Fraxinus excelsior. Mol. Ecol. 8: 160-163.Search in Google Scholar

BURKE, J. M. and M. L. ARNOLD (2001): Genetics and the fitness of hybrids. Ann. Rev. Genet. 35: 31-52.10.1146/annurev.genet.35.102401.08571911700276Search in Google Scholar

CLEMENT, M., D. POSADA and K. A. CRANDALL (2000): TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9: 1657-1660.Search in Google Scholar

CORNUET, J. M. and G. LUIKART (1996): Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014.10.1093/genetics/144.4.200112077478978083Search in Google Scholar

CUNDALL, E. P., C. M. CAHALAN and T. CONNOLLY (2003): Early results of ash (Fraxinus excelsior L.) provenance trials at sites in England and Wales. Forestry 76: 385-399.10.1093/forestry/76.4.385Search in Google Scholar

DOYLE, J. J. and J. L. DOYLE (1987): A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19: 11-15. Search in Google Scholar

EDMANDS, S. and C. C. TIMMERMAN (2003): Modeling factors affecting the severity of outbreeding depression. Cons. Biol. 17: 883-892.Search in Google Scholar

ELLISON, C. K. and R. S. BURTON (2008): Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution 62: 631-638.10.1111/j.1558-5646.2007.00305.x18081717Search in Google Scholar

ERIXON, P. and B. OXELMAN (2008): Reticulate or tree-like chloroplast DNA evolution in Sileneae (Caryophyllaceae)? Mol. Phylogen. Evol. 48: 313-325.Search in Google Scholar

EVANNO, G., S. REGNAUT and J. GOUDET (2005): Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14: 2611-2620.Search in Google Scholar

FELSENSTEIN, J. (2002): PHYLIP (Phylogeny Inference Package) version 3.6a3. Department of Genome Science, University of Washington, Seattle.Search in Google Scholar

FRANKHAM, R. (2010): Challenges and opportunities of genetic approaches to biological conservation Biol. Cons. 143: 1919-1927.10.1016/j.biocon.2010.05.011Search in Google Scholar

FRAXIGEN (2005): Ash species in Europe: biological characteristics and practical guidelines for sustainable use. Oxford Forestry Institute, University of Oxford, Oxford.Search in Google Scholar

FREY, J. E., B. FREY and D. FORCIOLI (2005): Quantitative assessment of heteroplasmy levels in Senecio vulgaris chloroplast DNA. Genetica 123: 255-261.10.1007/s10709-004-3711-y15954496Search in Google Scholar

GARCIA-DIAZ, A., R. OYA, A. SANCHEZ and F. LUQUE (2003): Effect of prolonged vegetative reproduction of olive tree cultivars (Olea europaea L.) in mitochondrial homoplasmy and heteroplasmy. Genome 46: 377-381.10.1139/g03-01712834053Search in Google Scholar

HEBEL, I., R. HAAS and A. DOUNAVI (2006): Genetic variation of common ash (Fraxinus excelsior L.) populations from provenance regions in southern Germany by using nuclear and chloroplast microsatellites. Silvae Genet. 55: 38-44.10.1515/sg-2006-0006Search in Google Scholar

HEUERTZ, M., X. VEKEMANS, J. F. HAUSMAN, M. PALADA and O. J. HARDY (2003): Estimating seed versus pollen dispersal from spatial genetic structure in the common ash. Mol. Ecol. 12: 2483-2495.Search in Google Scholar

HEUERTZ, M., S. FINESCHI, M. ANZIDEI, R. PASTORELLI, D. SALVINI, L. PAULE, N. FRASCARIA-LACOSTE, O. J. HARDY, X. VEKEMANS and G. G. VENDRAMIN (2004a): Chloroplast DNA variation and postglacial recolonization of common ash (Fraxinus excelsior L.) in Europe. Mol. Ecol. 13: 3437-3452.10.1111/j.1365-294X.2004.02333.x15488002Search in Google Scholar

HEUERTZ, M., J. F. HAUSMAN, O. J. HARDY, G. G. VENDRAMIN, N. FRASCARIA-LACOSTE and X. VEKEMANS (2004b): Nuclear microsatellites reveal contrasting patterns of genetic structure between western and southeastern European populations of the common ash (Fraxinus excelsior L.). Evolution 58: 976-988.10.1111/j.0014-3820.2004.tb00432.x15212379Search in Google Scholar

HEWITT, G. M. (2000): The genetic legacy of the Quaternary ice ages. Nature 405, 907-913.10.1038/3501600010879524Search in Google Scholar

HUNTLEY, B. and H. J. B. BIRKS (1983): An Atlas of Past and Present Pollen Maps for Europe, 0-13000 Years Ago. Cambridge University Press, Cambridge.Search in Google Scholar

JARAMILLO-CORREA, J. P. and J. BOUSQUET (2005): Mitochondrial genome recombination in the zone of contact between two hybridizing conifers Genetics 171: 1951-1962.10.1534/genetics.105.042770145611816118197Search in Google Scholar

JOHANSEN-MORRIS, A. D. and R. G. LATTA (2006): Fitness consequences of hybridization between ecotypes of Avena barbata: Hybrid breakdown, hybrid vigor, and transgressive segregation. Evolution 60: 1585-1595.10.1111/j.0014-3820.2006.tb00503.xSearch in Google Scholar

KORPEL’, Š . (1995): Die Urwälder der Westkarpaten. Gustav Fischer Verlag, Jena.Search in Google Scholar

KRAJ, W., M. ZAREK and T. KOWALSKI (2012): Genetic variability of Chalara fraxinea, dieback cause of European ash (Fraxinus excelsior L.). Mycol. Progress 11: 37-45.Search in Google Scholar

LATTA, R. G., K. M. GARDNER and A. D. JOHANSEN-MORRIS (2007): Hybridization, recombination, and the genetic basis of fitness variation across environments in Avena barbata. Genetica 129: 167-177.10.1007/s10709-006-9012-x17006737Search in Google Scholar

LEFORT, F., S. BRACHET, N. FRASCARIA-LACOSTE, K. J. EDWARDS and G. C. DOUGLAS (1999): Identification and characterisation of microsatellite loci in ash (Fraxinus excelsior L.) and their conservation in the olive family (Oleaceae). Mol. Ecol. 8: 1088-1091.Search in Google Scholar

LIEPELT, S., R. BIALOZYT and B. ZIEGENHAGEN (2002): Wind-dispersed pollen mediates postglacial gene flowamong refugia. Proc. Natl. Acad. Sci. USA 99: 14590-14594. 10.1073/pnas.21228539913792712391327Search in Google Scholar

LUIKART, G., W. B. SHERWIN, B. M. STEELE and F.W. ALLENDORF (1998): Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol. Ecol. 7: 963-974.Search in Google Scholar

MAGRI, D., G. G. VENDRAMIN, B. COMPS et al. (2006): Palaeobotanical and genetic data outline the Quaternaryhistory of European beech populations. New Phytologist 171: 199-222.10.1111/j.1469-8137.2006.01740.x16771995Search in Google Scholar

MALLET, J. (2005): Hybridization as an invasion of the genome. Trends Ecol. Evol. 20: 229-237.Search in Google Scholar

NEI, M. and W. H. LI (1979): Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. USA 76: 5269-5273.10.1073/pnas.76.10.5269413122291943Search in Google Scholar

PETIT, R. J., S. BREWER, S. BORDÁCS et al. (2002): Identification of refugia and post-glacial colonization routes of European white oaks based on chloroplast DNA and fossil pollen evidence. For. Ecol. Manage. 156: 49-74.Search in Google Scholar

PLANTE, F. and L. BERNIER (1997): Variability of virulence of Nectria galligena towards northern hardwoods Eur. J. For. Pathol. 27: 261-272.10.1111/j.1439-0329.1997.tb00868.xSearch in Google Scholar

PLIURA, A. and V. BALIUCKAS (2007): Genetic variation in adaptive traits of progenies of Lithuanian and western European populations of Fraxinus excelsior L. Baltic Forestry 13: 28-38.Search in Google Scholar

PONS, O. and R. J. PETIT (1996): Measuring and testing genetic differentiation with ordered versus unordered alleles Genetics 144: 1237-1245.10.1093/genetics/144.3.123712076158913764Search in Google Scholar

PRITCHARD, J. K., M. STEPHENS and P. DONNELLY (2000): Inference of population structure using multilocus genotype data. Genetics 155: 945-959.10.1093/genetics/155.2.945146109610835412Search in Google Scholar

RIESEBERG, L. H. and S. E. CARNEY (1998): Plant hybridization. New Phytologist 140: 599-624.10.1046/j.1469-8137.1998.00315.x33862960Search in Google Scholar

ROBERTSON, K. R., J. B. PHIPPS, J. R. ROHRER and P. G. SMITH (1991): A synopsis of genera in Maloideae (Rosaceae). Syst. Bot. 16: 376-394.Search in Google Scholar

ROSAS, U., N. H. BARTON, L. COPSEY, P. B. de REUILLE and E. COEN (2010): Cryptic variation between species and the basis of hybrid performance. PLoS Biology 8: e1000429.10.1371/journal.pbio.1000429290729320652019Search in Google Scholar

ROSENBERG, N. A., J. K. PRITCHARD, J. L WEBER, H. M. CANN, K. K KIDD, L. A. ZHIVOTOVSKY and M.W. FELDMAN (2002): Genetic structure of human populations. Science 298: 2381-2385.10.1126/science.107831112493913Search in Google Scholar

SAMBATTI, J. B. M., D. ORTIZ-BARRIENTOS, E. J. BAACK and L. H. RIESEBERG (2008): Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. Ecology Lett 11: 1082-1091.10.1111/j.1461-0248.2008.01224.x273736518643842Search in Google Scholar

SCHNEIDER, S., D. ROESSLI and L. EXCOFFIER (2000): Arlequin: A software for population genetic data. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandSearch in Google Scholar

SLATKIN, M. (1995): A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457-462.10.1093/genetics/139.1.45712063437705646Search in Google Scholar

SUTHERLAND, B. G., A. BELAJ, S. NIER, J. E. COTTRELL, S. P. VAUGHAN, J. HUBERT and K. RUSSELL (2010): Molecular biodiversity and population structure in common ash (Fraxinus excelsior L.) in Britain: implications for conservation. Mol. Ecol. 19: 2196-211.Search in Google Scholar

SZYMURA, J. M. and N. H. BARTON (1986): Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and Bombina variegata, near Cracow in southern Poland. Evolution 40: 1141-1159.Search in Google Scholar

WEISING, K. and R. C. GARDNER (1999: A set of conserved PCR primers for the analysis of simple repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42: 9-19.10.1139/g98-104Search in Google Scholar

WOLOSZYNSKA, M. (2010): Heteroplasmy and stoichiometric complexity of plant mitochondrial genomes - though this be madness, yet there’s method in’t. J. Exp. Bot. 61: 657-671.Search in Google Scholar

ZWIERZYKOWSKI, Z., R. TAYYAR, M. BRUNELL and A. J. LUKASZEWSKI (1998): Genome recombination in intergeneric hybrids between tetraploid Festuca pratensis and Lolium multiflorum. J. Hered. 89: 324-328.10.1093/jhered/89.4.324Search in Google Scholar

Recommended articles from Trend MD

Plan your remote conference with Sciendo