Skip to main content
SpringerLink
Log in

Interspecific hybridisation and interaction with cultivars affect the genetic variation of Ulmus minor and Ulmus glabra in Flanders

  • Original Paper
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Interspecific hybridisation and gene flow from cultivated plants may have profound effects on the evolution of wild species. Considering the cultural history and past use of Ulmus minor and Ulmus glabra trees in Flanders (northern Belgium), we investigated the extent of human impact on the genetic variation of the remaining, supposedly indigenous elm populations. We therefore examined the rate of interspecific hybridisation, which is expected to be higher under human influence, the occurrence of clones within and among locations, the presence of cultivars and their possible offspring. Based on results produced using 385 amplified fragment length polymorphic (AFLP) markers, 46 % of the 106 investigated Flemish elms appeared to be F1 hybrids or backcrosses to one of the parent species, while no F2 hybrids (F1 × F1 progeny) were found. Clonality was mainly found among U. minor and hybrids, which are more likely to form root suckers or sprouts as opposed to U. glabra. The majority of the studied locations (76 % of the locations with multiple samples) showed evidence of clonal reproduction. Several, sometimes distant, locations shared a multilocus lineage. We also found indications of gene flow from cultivated elms into native species. It is conceivable that reproductive material has been moved around extensively, obscuring the natural genetic structure of the elm populations. The results help guide the Flemish elm genetic resources conservation programme.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Achard S (2012) Brainwaver: basic wavelet analysis of multivariate time series with a visualisation and parametrisation using graph theory. R package version 1.6 edn

  • Aerts R, Berecha G, Gijbels P, Hundera K, Van Glabeke S, Vandepitte K, Muys B, Roldán-Ruiz I, Honnay O (2013) Genetic variation and risks of introgression in the wild Coffea arabica gene pool in south-western Ethiopian montane rainforests. Evol Appl 6:243–252. doi:10.1111/j.1752-4571.2012.00285.x

    Article  PubMed Central  PubMed  Google Scholar 

  • Anderson EC (2008) Bayesian inference of species hybrids using multilocus dominant genetic markers. Philos Trans R Soc B 363:2841–2850

    Article  Google Scholar 

  • Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229

    CAS  PubMed Central  PubMed  Google Scholar 

  • Anderson J, Churchill G, Autrique J, Tanksley S, Sorrells M (1993) Optimizing parental selection for genetic linkage maps. Genome 36:181–186

    Article  CAS  PubMed  Google Scholar 

  • Arnaud-Haond S, Alberto F, Teixeira S, Procaccini G, Serrao EA, Duarte CM (2005) Assessing genetic diversity in clonal organisms: low diversity or low resolution? Combining power and cost efficiency in selecting markers. J Hered 96:434–440

    Article  CAS  PubMed  Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, USA

    Google Scholar 

  • Arrigo N, Tuszynski JW, Ehrich D, Gerdes T, Alvarez N (2009) Evaluating the impact of scoring parameters on the structure of intra-specific genetic variation using RawGeno, an R package for automating AFLP scoring. BMC Bioinforma 10:33. doi:10.1186/1471-2105-10-33

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300

    Google Scholar 

  • Bonin A, Bellemain E, Eidesen PB, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273

    Article  CAS  PubMed  Google Scholar 

  • Brasier CM (2001) Rapid evolution of introduced plant pathogens via interspecific hybridization. Bioscience 51:123–133. doi:10.1641/0006-3568(2001)051[0123:reoipp]2.0.co;2

    Article  Google Scholar 

  • Brundu G, Lupi R, Zapelli I, Fossati T, Patrignani G, Camarda I, Sala F, Castiglione S (2008) The origin of clonal diversity and structure of Populus alba in Sardinia: evidence from nuclear and plastid microsatellite markers. Ann Bot 102:997–1006. doi:10.1093/aob/mcn192

    Article  PubMed Central  PubMed  Google Scholar 

  • Brunet J, Zalapa J, Pecori F, Santini A (2013) Hybridization and introgression between the exotic Siberian elm, Ulmus pumila, and the native Field elm, U. minor, in Italy. Biol Invasions:1–14. doi:10.1007/s10530-013-0486-z

  • Burgess KS, Morgan M, Deverno L, Husband BC (2005) Asymmetrical introgression between two Morus species (M. alba, M. rubra) that differ in abundance. Mol Ecol 14:3471–3483. doi:10.1111/j.1365-294X.2005.02670.x

    Article  CAS  PubMed  Google Scholar 

  • Cogolludo-Agustin MA, Agundez D, Gil L (2000) Identification of native and hybrid elms in Spain using isozyme gene markers. Heredity 85:157–166. doi:10.1046/j.1365-2540.2000.00740.x

    Article  CAS  PubMed  Google Scholar 

  • Collin E (2002) Strategies and guidelines for the conservation of the genetic resources of Ulmus spp. In: Turok J, Eriksson G, Russell K, Borelli S (eds) Noble Hardwoods Network, Report of the fourth meeting, September 1999, Gmunden, Austria, and the fifth meeting, May 2001, Blessington. Ireland. International Plant Genetic Resources Institute, Rome, Italy, pp 50–67

    Google Scholar 

  • Corander J, Marttinen P, Siren J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinforma 9:539. doi:10.1186/1471-2105-9-539

    Article  Google Scholar 

  • de Meeûs T, Balloux F (2004) Clonal reproduction and linkage disequilibrium in diploids: a simulation study. Infect Genet Evol 4:345–351. doi:10.1016/j.meegid.2004.05.002

    Article  PubMed  Google Scholar 

  • Douhovnikoff V, Dodd RS (2003) Intra-clonal variation and a similarity threshold for identification of clones: application to Salix exigua using AFLP molecular markers. Theor Appl Genet 106:1307–1315. doi:10.1007/s00122-003-1200-9

    CAS  PubMed  Google Scholar 

  • Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475. doi:10.1111/j.1365-294X.2006.03148.x

    Article  PubMed  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci 97:7043–7050. doi:10.1073/pnas.97.13.7043

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Elwes HJ, Henry A (1906) The trees of Great Britain & Ireland / by Henry John Elwes and Augustine Henry, vol 7. Priv. print., Edinburgh. doi:10.5962/bhl.title.17123

  • Flint-Garcia SA, Thornsberry JM, S E, IV B (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374. doi:doi:10.1146/annurev.arplant.54.031902.134907

  • Forster ES, Heffner E (1954) Lucius Junius Moderatus Columella: on agriculture II. Harvard University Press, Cambridge, Mass

    Google Scholar 

  • Fuentes-Utrilla P, Lopez-Rodriguez RA, Gil L (2004) The historical relationship of elms and vines. Invest Agrar: Sist Recur For 13:7–15

    Google Scholar 

  • Fussi B, Bonello J, Calleja E, Heinze B (2012) Combining the use of molecular techniques and archival documentary evidence to trace the origin of Populus alba in a Central Mediterranean archipelago. Eur J For Res 131:347–354. doi:10.1007/s10342-011-0506-4

    Article  Google Scholar 

  • Gil L, Fuentes-Utrilla P, Soto A, Cervera MT, Collada C (2004) English elm is a 2,000-year-old Roman clone. Nature 431:1053. doi:10.1038/4311053a

    Article  CAS  PubMed  Google Scholar 

  • Gómez A, Carvalho GR (2000) Sex, parthenogenesis and genetic structure of rotifers: microsatellite analysis of contemporary and resting egg bank populations. Mol Ecol 9:203–214. doi:10.1046/j.1365-294x.2000.00849.x

    Article  PubMed  Google Scholar 

  • Goodall-Copestake WP, Hollingsworth ML, Hollingsworth PM, Jenkins GI, Collin E (2005) Molecular markers and ex situ conservation of the European elms (Ulmus spp.). Biol Conserv 122:537–546

    Article  Google Scholar 

  • Goodman SJ, Barton NH, Swanson G, Abernethy K, Pemberton JM (1999) Introgression through rare hybridization: a genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll, Scotland. Genetics 152:355–371

    CAS  PubMed Central  PubMed  Google Scholar 

  • Grant PR, Grant BR (1994) Phenotypic and genetic effects of hybridization in Darwin's finches. Evolution 48:297–316

    Article  Google Scholar 

  • Halkett F, Simon J-C, Balloux F (2005) Tackling the population genetics of clonal and partially clonal organisms. Trends Ecol Evol 20:194–201. doi:10.1016/j.tree.2005.01.001

    Article  PubMed  Google Scholar 

  • Haubold B, Hudson RR (2000) LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics 16:847–849. doi:10.1093/bioinformatics/16.9.847

    Article  CAS  PubMed  Google Scholar 

  • Haubold B, Travisano M, Rainey PB, Hudson RR (1998) Detecting linkage disequilibrium in bacterial populations. Genetics 150:1341-1348

    Google Scholar 

  • Heybroek HM (1993) The Dutch elm breeding program. In: Sticklen MB, Sherald JL (eds) Dutch Elm Disease research. Springer, New York, pp 16–25. doi:10.1007/978-1-4615-6872-8_3

    Chapter  Google Scholar 

  • Heybroek HM, Goudzwaard L, Kaljee H (2009) Iep of Olm: karakterboom van de Lage Landen. KNNV Uitgeverij, Zeist, the Netherlands

    Google Scholar 

  • Honnay O, Jacquemyn H (2008) A meta-analysis of the relation between mating system, growth form and genotypic diversity in clonal plant species. Evol Ecol 22:299–312. doi:10.1007/s10682-007-9202-8

    Article  Google Scholar 

  • Jones OR, Wang J (2009) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555. doi:10.1111/j.1755-0998.2009.02787.x

    Article  PubMed  Google Scholar 

  • Jump AS, Peñuelas J (2006) Genetic effects of chronic habitat fragmentation in a wind-pollinated tree. Proc Natl Acad Sci U S A 103:8096–8100. doi:10.1073/pnas.0510127103

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kron P, Husband BC (2009) Hybridization and the reproductive pathways mediating gene flow between native Malus coronaria and domestic apple M. domestica. Botany 87:864–874. doi:10.1139/B09-045

    Article  CAS  Google Scholar 

  • Laikre L, Schwartz MK, Waples RS, Ryman N, GeM WG (2010) Compromising genetic diversity in the wild: unmonitored large-scale release of plants and animals. Trends Ecol Evol 25:520–529

    Article  PubMed  Google Scholar 

  • Lambinon J, De Langhe J-E, Delvosalle L, Duvigneaud J (1998) Flora of Belgium, Luxembourg, Northern France and neighboring areas (pteridophyta and spermatophyta), 3rd edn. National Botanic Garden of Belgium, Meise

    Google Scholar 

  • Lepais O, Petit RJ, Guichoux E, Lavabre JE, Alberto F, Kremer A, Gerber S (2009) Species relative abundance and direction of introgression in oaks. Mol Ecol 18:2228–2242

    Article  CAS  PubMed  Google Scholar 

  • Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629

    Article  Google Scholar 

  • Maes B (2006) Inheemse bomen en struiken in Nederland en Vlaanderen: herkenning, verspreiding, geschiedenis en gebruik. Boom, Utrecht

    Google Scholar 

  • Mariette S, Tavaud M, Arunyawat U, Capdeville G, Millan M, Salin F (2010) Population structure and genetic bottleneck in sweet cherry estimated with SSRs and the gametophytic self-incompatibility locus. BMC Genet 11:77

    Article  PubMed Central  PubMed  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Belknap Press of Harvard University Press, Harvard

    Book  Google Scholar 

  • McKey D, Elias M, Pujol B, Duputié A (2010) The evolutionary ecology of clonally propagated domesticated plants. New Phytol 186:318–332. doi:10.1111/j.1469-8137.2010.03210.x

    Article  PubMed  Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Mittempergher L, La Porta N (1991) Hybridization studies in the Eurasian species of elm (Ulmus spp.). Silvae Genet 40:237–243

    Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nielsen LR, Kjaer ED (2010) Gene flow and mating patterns in individuals of wych elm (Ulmus glabra) in forest and open land after the influence of Dutch elm disease. Conserv Genet 11:257–268

    Article  Google Scholar 

  • Poncet BN, Herrmann D, Gugerli F, Taberlet P, Holderegger R, Gielly L, Rioux D, Thuiller W, Aubert S, Manel S (2010) Tracking genes of ecological relevance using a genome scan in two independent regional population samples of Arabis alpina. Mol Ecol 19:2896–2907

    Article  CAS  PubMed  Google Scholar 

  • Potts BM, Barbour RC, Hingston AB, Vaillancourt RE (2003) Turner review no. 6. Genetic pollution of native eucalypt gene pools—identifying the risks. Aust J Bot 51:1–25. doi:10.1071/BT02035

    Article  Google Scholar 

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Rhymer JM, Simberloff D (1996) Estintction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Richens RH (1983) Elm. Cambridge University Press, Cambridge

    Google Scholar 

  • Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389. doi:10.2307/2952498

    Article  Google Scholar 

  • Santos-del-Blanco L, de-Lucas A, González-Martínez S, Sierra-de-Grado R, Hidalgo E (2013) Extensive clonal assemblies in Populus alba and Populus x canescens from the Iberian Peninsula. Tree Genet Genom 9:499–510. doi:10.1007/s11295-012-0574-8

    Article  Google Scholar 

  • Smulders MJM, Beringen R, Volosyanchuk R, Vanden Broeck A, Schoot J, Arens P, Vosman B (2008) Natural hybridisation between Populus nigra L. and P. x canadensis Moench. Hybrid offspring competes for niches along the Rhine river in the Netherlands. Tree Genet Genom 4:663–675. doi:10.1007/s11295-008-0141-5

    Article  Google Scholar 

  • Stronen AV, Paquet PC (2013) Perspectives on the conservation of wild hybrids. Biol Conserv 167:390–395. doi:10.1016/j.biocon.2013.09.004

    Article  Google Scholar 

  • Tibayrenc M, Kjellberg F, Arnaud J, Oury B, Brenière SF, Dardé ML, Ayala FJ (1991) Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc Natl Acad Sci 88:5129–5133. doi:10.1073/pnas.88.12.5129

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Touw A (1963) Een voorlopig overzicht van de Nederlandse Iepen. Jb Ned Dendrologische Vereniging 22:57–72

    Google Scholar 

  • Townsend AM (1975) Crossability patterns and morphological variation among elm species and hybrids. Silvae Genet 24:18–23

    Google Scholar 

  • Turelli M, Orr HA (2000) Dominance, epistasis and the genetics of postzygotic isolation. Genetics 154:1663–1679

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vähä J-P, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72

    Article  PubMed  Google Scholar 

  • Vallejo-Marín M, Dorken ME, Barrett SC (2010) The ecological and evolutionary consequences of clonality for plant mating. Ann Rev Ecol Evol Syst 41:193–213

    Article  Google Scholar 

  • van Dissel ED (1912) De storm van 30 sept.-1 Oct. 1911 in het Haagsche bosch. Staatsbosbeheer, Utrecht

    Google Scholar 

  • Vanden Broeck A, Cox K, Villar M (2012) Natural hybridization and potential seed set of sympatric Populus nigra and Populus x canadensis along the river IJzer in Flanders (Belgium). Plant Ecol Evol 145:341–349. doi:10.5091/plecevo.2012.677

    Article  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Vandelee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) Aflp—a new technique for DNA-fingerprinting. Nucleic Acids Res 23:4407–4414

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang J, Santure AW (2009) Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181:1579–1594. doi:10.1534/genetics.108.100214

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Webber JF (2004) Experimental studies on factors influencing the transmission of Dutch elm disease. Invest Agrar: Sist Recur For 13:197–205

    Google Scholar 

  • Wirtz P (1999) Mother species–father species: unidirectional hybridization in animals with female choice. Anim Behav 58:1–12. doi:10.1006/anbe.1999.1144

    Article  PubMed  Google Scholar 

  • Zalapa JE, Brunet J, Guries RP (2009) Patterns of hybridization and introgression between invasive Ulmus pumila (Ulmaceae) and native U. rubra. Am J Bot 96:1116–1128. doi:10.3732/ajb.0800334

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank B. Maes for providing us with samples and useful information. Also, many thanks to Leen Verschaeve, Nancy Van Liefferinge, An Van Breusegem, David Halfmaerten and Sabrina Neyrinck (INBO) for the laboratory assistance and Stefaan Moreels (INBO) for his help in collecting the samples and creating the Flemish elm gene bank. Finally, we thank the reviewers for their insightful comments.

Data archiving statement

AFLP data: data available from the Dryad Digital Repository: http://doi.org/10.5061/dryad.4554j.

Author information

Authors and Affiliations

  1. Research Institute for Nature and Forest, Gaverstraat 4, 9500, Geraardsbergen, Belgium

    Karen Cox, An Vanden Broeck, Kristine Vander Mijnsbrugge & Joachim Mergeay

  2. Centre for Genetic Resources, the Netherlands (CGN), PO box 47, 6700AA, Wageningen, The Netherlands

    Joukje Buiteveld

  3. Irstea, UR EFNO, Centre de Nogent-sur-Vernisson, 45290, Nogent-sur-Vernisson, France

    Eric Collin

  4. Dorschkamp Forest Research Station, Wageningen, Jonkerlaan 90-113, 2242 EX, Wassenaar, The Netherlands

    Hans M. Heybroek

Authors
  1. Karen Cox
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. An Vanden Broeck
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kristine Vander Mijnsbrugge
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joukje Buiteveld
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eric Collin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hans M. Heybroek
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Joachim Mergeay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karen Cox.

Additional information

Communicated by S. C. González-Martínez

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Best maximum likelihood sibship assignment plot of the sibship structure for the unique ramets of Flemish multilocus lineages of the U. minor-U. glabra complex obtained with Colony v2.0.1.9. Above diagonal (black dots): full-sibs; below diagonal (grey dots): half-sibs. On both axes, the location code of each individual is given (PDF 37 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cox, K., Vanden Broeck, A., Vander Mijnsbrugge, K. et al. Interspecific hybridisation and interaction with cultivars affect the genetic variation of Ulmus minor and Ulmus glabra in Flanders. Tree Genetics & Genomes 10, 813–826 (2014). https://doi.org/10.1007/s11295-014-0722-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-014-0722-4

Keywords

Search

Navigation