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Annals of Forest Science

, 75:98 | Cite as

Genetic evidence of human mediated, historical seed transfer from the Tyrolean Alps to the Romanian Carpathians in Larix decidua (Mill.) forests

  • Hannes Raffl
  • Heino Konrad
  • Lucian A. Curtu
  • Thomas Geburek
Research Paper

Abstract

Key message

Historic transfer of larch from Alpine sources to Southern and Eastern Carpathians has been verified by means of nuclear genetic markers. Tyrolean populations can be differentiated into a north-western and south-eastern group, while Romanian populations are separated according to the Southern and Eastern Carpathians. Low-level introgression from Alpine sources is found in autochthonous Carpathian populations.

Context

Large scale human mediated transfer of forest reproductive material may have strongly modified the gene pool of European forests. Particularly in European larch, large quantities of seeds from Central Europe were used for plantations in Southern and Eastern Europe starting in the mid nineteenth century.

Aims

Our main objective was to provide DNA marker based evidence for the anthropogenic transfer of Alpine larch reproductive material to native Carpathian populations.

Methods

We studied and compared 12 populations (N = 771) of Larix decidua in the Alps (Austria, Italy) and in the Southern and Eastern Carpathians (Romania) using 13 microsatellites.

Results

High genetic diversity (He = 0.752; RS = 9.4) and a moderate genetic differentiation (FST = 0.13; GST = 0.28) among populations were found; Alpine and Carpathian populations were clearly separated by clustering methods. A Tyrolean origin of plant material was evident for one out of four adult Romanian populations. In the transferred population, a genetic influence from Carpathian sources was found neither in adults nor in juveniles, while the natural regeneration of two Romanian populations was genetically affected by Alpine sources to a minor degree (2.2 and 2.9% allochthonous individuals according to GeneClass and Structure, respectively).

Conclusion

Tracing back of plant transfer by means of genetic tools is straightforward, and we propose further studies to investigate gene flow between natural and transferred populations.

Keywords

Genetic pollution Genetic swamping Intraspecific introgression Microsatellites Spatial genetic structure 

Notes

Acknowledgements

We thank the forestry authority of the Autonomous Province of Bolzano and North Tyrol for providing information about the spatial position of larch stands and Manuel Fauner for his support in the field. Thomas Thalmayr helped to create figures. Christoph Dobeš provided an R script to calculate FST and GST among population groups. We also gratefully acknowledge the input of the handling editor Bruno Fady and three anonymous reviewers.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13595_2018_776_MOESM1_ESM.docx (130 kb)
ESM 1 (DOCX 130 kb)

References

  1. Androsiuk P, Shimono A, Westin J, Lindgren D, Fries A, Wang XR (2013) Genetic status of Norway spruce (Picea abies) breeding populations for northern Sweden. Silvae Genet 62:127–136CrossRefGoogle Scholar
  2. Baudouin L, Lebrun P (2000) An operational Bayesian approach for the identification of sexually reproduced cross-fertilized populations using molecular markers. Acta Hortic 546:81–93Google Scholar
  3. Belletti P, Ferrazzini D, Piotti A, Monteleone I, Ducci F (2012) Genetic variation and divergence in Scots pine (Pinus sylvestris L.) within its natural range in Italy. Eur J For Res 131:1127–1138CrossRefGoogle Scholar
  4. Brown KR, Zobel DB, Zasada JC (1988) Seed dispersal, seedling emergence, and early survival of Larix laricina (Du Roi) K. Koch in the Tanana Valley, Alaska. Can J For Res 18:306–314CrossRefGoogle Scholar
  5. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631CrossRefGoogle Scholar
  6. Chybicki IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. J Hered 100:106–113CrossRefGoogle Scholar
  7. Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000PubMedPubMedCentralGoogle Scholar
  8. Development Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  9. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  10. Dietrichson J (1991) Genspredning fra plantet mellomeuropeisk gran (Picea abies [L.] Karst.) på Syd-Østlandet. Rapport fra Skogforsk 11:1–11Google Scholar
  11. Dzialuk A, Chybicki I, Gout R, Mączka T, Fleischer P, Konrad H, Curtu AL, Sofletea N, Valadon A (2014) No reduction in genetic diversity of Swiss stone pine (Pinus cembra L.) in Tatra Mountains despite high fragmentation and small population size. Conserv Genet 15:1433–1445CrossRefGoogle Scholar
  12. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  13. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefGoogle Scholar
  14. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567CrossRefGoogle Scholar
  15. Fady B, Aravanopoulos FA, Alizoti P, Mátyás C, von Wühlisch G, Westergren M, Belletti P, Cvjetkovic B, Ducci F, Huber G, Kelleher CT, Khaldi A, Kharrat MBD, Kraigher H, Kramer K, Mühlethaler U, Peric S, Perry A, Rousi M, Sbay H, Stojnic S, Tijardovic M, Varela MC, Vendramin GG, Zlatanov T (2016) Evolution-based approach needed for the conservation and silviculture of peripheral forest tree populations. For Ecol Manag 375:66–75CrossRefGoogle Scholar
  16. Felsenstein J (1989) Phylip—phylogeny inference package vers. 32 Cladistics 5:164–166Google Scholar
  17. Frankham R, Ballou JD, Ralls K, MDB E, Dudash MR, Fenster CB, Lacy RC, Sunnucks P (2017) Genetic management of fragmented animal and plant populations. Oxford University Press, United Kingdom 400 pCrossRefGoogle Scholar
  18. Fujio Y, von Brand E (1991) Differences in degree of homozygosity between seed and sown populations of the Japanese scallop Patinopecten yessoensis. Nippon Suisan Gakk 57:45–50CrossRefGoogle Scholar
  19. Gava M (1963) Le meleze Roumanie. Rev For Fr 6:541–545CrossRefGoogle Scholar
  20. Geburek T, Robitscheck K, Milasowski N, Schadauer C (2007) Different cone colour pay off: lessons learnt from European larch (Larix decidua Mill.) and Norway spruce (Picea abies [Karst.] L.). Can J Bot 85:132–140CrossRefGoogle Scholar
  21. Gothe H (1961) Samenkundliche und pflanzenzüchterische Untersuchungen an der Schlitzer Lärche. PhD Thesis University of Munich, Munich, p 136Google Scholar
  22. Goudet J (1995) Fstat vers. 1.2: a computer programme to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  23. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  24. Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318CrossRefGoogle Scholar
  25. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638CrossRefGoogle Scholar
  26. Heiss A, Kofler W, Oeggl K (2005) The Ulten Valley in South Tyrol, Italy: vegetation and settlement history of the area, and macrofossil record from the Iron Age cult site of St. Walburg. Palyno-Bull. Inst Bot Univ Innsbruck 1:63–73Google Scholar
  27. Heller R, Siegismund HR (2009) Relationship between three measures of genetic differentiation G ST, D EST and GST: how wrong have we been? Mol Ecol 18:2080–2083CrossRefGoogle Scholar
  28. Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Tr Ecol Evol 18:147–155CrossRefGoogle Scholar
  29. Jansen S, Geburek T (2016) Historic translocations of European larch (Larix decidua Mill.) genetic resources across Europe—a review from the 17th until the mid-20th century. For Ecol Manag 379:114–123CrossRefGoogle Scholar
  30. Kettle CJ, Hollingsworth PM, Jaffre T, Moran B, Ennos RA (2007) Identifying the early genetic consequences of habitat degradation in a highly threatened tropical conifer, Araucaria nemorosa Laubenfels. Mol Ecol 16:3581–3591CrossRefGoogle Scholar
  31. 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 15:3907–3918CrossRefGoogle Scholar
  32. King GM, Gugerli F, Fonti P, Frank DC (2013) Tree growth response along an elevational gradient: climate or genetics? Oecologia 173:1587–1600CrossRefGoogle Scholar
  33. Knowles P, Perry DJ, Foster HA (1992) Spatial genetic structure in two tamarack [Larix laricina (Du Roi) K. Koch] populations with differing establishment histories. Evolution 46:572–576CrossRefGoogle Scholar
  34. Konrad H (2018) RawDataRaffletal_Larix. V 22 Aug. 2018. OSF. [Dataset]. https://doi.org/10.17605/OSF.IO/37RYM. Google Scholar
  35. Kopp M, Matuszewski S (2014) Rapid evolution of quantitative traits: theoretical perspectives. Evol Appl 7:169–191CrossRefGoogle Scholar
  36. Kremer A, Ronce O, Robledo-Arnuncio JJ, Guillaume F, Bohrer G, Nathan R, Bridle JR, Gomulkiewicz R, Klein EK, Ritland K, Kuparinen A, Gerber S, Schueler S (2012) Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecol Lett 15:378–392CrossRefGoogle Scholar
  37. Larionova AY, Yakhneva NV, Abaimov AP (2004) Genetic diversity and differentiation of Gmelin larch Larix gmelinii populations from Evenkia (Central Siberia). Russ J Genet 40:1127–1134CrossRefGoogle Scholar
  38. Leblois R (2011) Assignment and Clustering algorithms for individual multilocus genotypes. Centre de Biologie et de Gestion des Populations. Erasmus Mundus Master Programme in Evolutionary Biology, University Montpellier II: Genetic Data Analysis, 2012-2013. Montpellier. France. Available from http://raphael.leblois.free.fr/ressources/cours/MEME_30-03-2011_Clustering_LEBLOIS_small.pdf. Accessed 15 Dec 2017
  39. Lendvay B, Höhn M, Brodbeck S, Mîndrescu M, Gugerli F (2014) Genetic structure in Pinus cembra from the Carpathian Mountains inferred from nuclear and chloroplast microsatellites confirms post-glacial range contraction and identifies introduced individuals. Tree Genet Genom 10:1419–1433CrossRefGoogle Scholar
  40. Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425CrossRefGoogle Scholar
  41. Luikart G, Allendorf FW, Cornuet J-M, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247CrossRefGoogle Scholar
  42. Magyari EK, Jakab G, Bálint M, Kern Z, Buczkó K, Braun M (2012) Rapid vegetation response to Lateglacial and early Holocene climatic fluctuation in the South Carpathian Mountains (Romania). Quat Sci Rev 35:116–130CrossRefGoogle Scholar
  43. Maier J (1992) Herkunftsunterschiede in der Länge der Stomatareihen bei Larix decidua Mill. Flora 186:169–176CrossRefGoogle Scholar
  44. Mayer H (1992) Waldbau auf soziologisch-ökologischer Grundlage. Gustav Fischer, StuttgartGoogle Scholar
  45. Nei M (1972) Genetic distance between populations. Am Nat 106:283–292CrossRefGoogle Scholar
  46. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedPubMedCentralGoogle Scholar
  47. Nishimura M, Setoguchi H (2011) Homogeneous genetic structure and variation in tree architecture of Larix kaempferi along altitudinal gradients on Mt. Fuji. J Plant Res 124:253–263CrossRefGoogle Scholar
  48. Oeggl K, Wahlmüller N (1994) Holozäne Vegetationsentwicklung an der Waldgrenze der Ostalpen: die Plancklacke (2140m)/Sankt Jakob im Defreggen, Osttirol. Diss Bot 234:389–411Google Scholar
  49. Oreshkova NV, Belokon MM, Jamiyansuren S (2013) Genetic diversity, population structure, and differentiation of Siberian Larch, Gmelin Larch, and Cajander Larch on SSR marker data. Russ J Genet 49:178–186CrossRefGoogle Scholar
  50. Øyen B (2006) Lerk (Larix) i Norge – del. Dyrkningshistorien Aktuelt fra skogforskningen 2:1–16Google Scholar
  51. Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation based exploration of accuracy and power. Mol Ecol 13:55–65CrossRefGoogle Scholar
  52. Pâques LE, Foffová E, Heinze B, Lelu-Walter M-A, Liesebach M, Philippe G (2013) Larches (Larix sp.). In: Pâques LE (ed) Forest tree breeding in Europe; current state-of-the-art and perspectives, managing forest ecosystems. Springer Science & Business Media, p 13–122Google Scholar
  53. Pardé J (1957) Plaidoyer pour Mélèze. Rev For Franç 9:634–650CrossRefGoogle Scholar
  54. Pazouki L, Shanjani PS, Fields PD, Martins K, Suhhorutšenko M, Viinalass H, Niinemets Ü (2016) Large within-population genetic diversity of the widespread conifer Pinus sylvestris at its soil fertility limit characterized by nuclear and chloroplast microsatellite markers. Eur J For Res 135:161–177CrossRefGoogle Scholar
  55. Peakall ROD, Smouse PE (2006) GENEALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  56. Peakall ROD, Smouse PE (2012) GENEALEX 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefGoogle Scholar
  57. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  58. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539CrossRefGoogle Scholar
  59. Pluess AR (2011) Pursuing glacier retreat: genetic structure of a rapidly expanding Larix decidua population. Mol Ecol 20:473–485CrossRefGoogle Scholar
  60. Porth I, El-Kassaby YA (2014) Assessment of the genetic diversity in forest tree populations using molecular markers. Diversity 6:283–295CrossRefGoogle Scholar
  61. Pritchard JK, Stephens P, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  62. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  63. Rousset F (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Res 8:103–106CrossRefGoogle Scholar
  64. Rubner K, Svoboda P (1944) Untersuchungen an Lärchenzapfen verschiedener Herkunft. Intersylva 4:121–146Google Scholar
  65. Rubţov S (1965) Arealui si ecologia Laricelui - Centrele de raspindire naturala a laricelui in Romania. In: Rubţov S (ed) Laricele - Ecologia si Cultura. Editura Agro-Silvica, p 65–74Google Scholar
  66. Rubţov S, Mocanu V (1958) Raspindirea laricelui spontan si cultivat, in R.P.R. St cerc biol 1:5–53Google Scholar
  67. Savolainen O, Kärkkäinen K, Kuittinen H (1992) Estimating numbers of embryonic lethals in conifers. Heredity 69:308–314CrossRefGoogle Scholar
  68. Simak M (1967) Seed weight of larch from different provenances (Larix decidua Mill.). Stud For Suec 57:1–31Google Scholar
  69. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:1463–1463PubMedCentralGoogle Scholar
  70. Stănescu V, Șofletea N, Popescu O (1997) Flora forestieră lemnoasă a României. Editura Ceres, BucureștiGoogle Scholar
  71. Stoeckel S, Grange J, Fernandez-Manjarres J, Biger I, Frascaria-Lacoste N, Mariette S (2006) Heterozygote excess in a self-incompatible and partially clonal forest tree species—Prunus avium L. Mol Ecol 15:2109–2118CrossRefGoogle Scholar
  72. Tollefsrud MM, Sønstebø JH, Brochmann C, Johnsen Ø, Skrøppa T, Vendramin GG (2009) Combined analysis of nuclear and mitochondrial markers provide new insight into the genetic structure of North European Picea abies. Heredity 102:549–562CrossRefGoogle Scholar
  73. Unger GM, Vendramin GG, Robledo-Arnuncio JJ (2014) Estimating exotic gene flow into native pine stands: zygotic vs. gametic components. Mol Ecol 23:5435–5447CrossRefGoogle Scholar
  74. van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  75. Wagner S (2013) History of the European larch (Larix decidua Mill.). Doctoral thesis. Rheinische Friedrich-Wilhelms-Universität Bonn and the Université Bordeaux I, Bonn and Bordeaux, 163 ppGoogle Scholar
  76. Wagner S, Gerber S, Petit RJ (2012) Two highly informative dinucleotide SSR multiplexes for the conifer Larix decidua (European larch). Mol Ecol Res 12:717–725CrossRefGoogle Scholar
  77. Wagner S, Liepelt S, Gerber S, Petit RJ (2015a) Within-range translocations and their consequences in European larch. PLoS One 10:e0127516.  https://doi.org/10.1371/journal.pone.0127516 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Wagner S, Litt T, Sànchez-Goni MF, Petit R (2015b) History of Larix decidua Mill. (European larch) since 130 ka. Quat Sci Rev 124:224–247CrossRefGoogle Scholar
  79. Weir BS, Cockerham CC (1984) Estimating F statistics for the analysis of population structure. Evolution 38:1358–1370PubMedGoogle Scholar
  80. Weisgerber H, Šindelár J (1992) IUFRO’s role in coniferous tree improvement. History, results, and future trends of research and international cooperation with European larch (Larix decidua Mill.). Silvae Genet 41:150–161Google Scholar
  81. Zhang G, Sun Z, Zhou D, Xiong M, Wang X, Yang J, Wei Z (2015) Development and characterization of novel EST-SSRs from Larix gmelinii and their cross-species transferability. Molecules 20:12469–12480CrossRefGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Forest GeneticsAustrian Research Centre for Forests (BFW)ViennaAustria
  2. 2.Department of ForestryTransilvania University of BrasovBrașovRomania

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