Skip to main content
SpringerLink
Log in

Implications of natural propagule flow for containment of genetically modified forest trees

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

Abstract

Propagule flow in populations of virtually all organisms has importance for both the genetic cohesion of the species and for its interaction with natural selection. It’s relevance` for the deployment of genetically modified organisms (GMOs) is that propagules can be expected to move, under a wide range of circumstances, and will carry transgenic elements with them. Any consideration of the potential risks of deploying GMOs in the wild must include an assessment of how far and how fast introduced elements are transferred to surrounding conspecific (and sometimes congeneric) populations. In practice, we need estimates of the rates/distances of both pollen and seed movement. There are analytical methods to characterize seed (maternity), pollen (paternity), and established offspring (parent-pair) data, but spatial limitations restrict the area that one can study, and these approaches require modification for application to propagule flow in GMOs. We can apply indirect methods to estimate male gamete dispersal based on pollen pool analysis for single mothers, when some degree of precision can be sacrificed in return for compensating gains in the spatial coverage, but the loss of precision is problematic for GMO tracking. Special methods have been developed for GMO tracking, and we shall show how to assess spatial movement of both transgene-carrying seeds and pollen and will illustrate with an example from Brassica napus, a well-studied crop species.

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

Similar content being viewed by others

References

  • Adams WT, Birkes DS (1989) Mating patterns in seed orchards. In: Proceedings of the 20th southern forest tree improvement conference, Charleston, pp. 75–86

  • Adams WT, Birkes DS (1991) Estimating mating patterns in forest tree populations. In: Fineschi S, Malvolti M, Cannata F, Hattemer H (eds) Biochemical markers in the population genetics of forest trees. SPB Academic Publishing, The Hague, Netherlands, pp 157–172

    Google Scholar 

  • Adams WT, Burczyk J (2000) Magnitude and implications of gene flow in gene conservation reserves. In: Boyle T, Boshier D, Young A (eds) Forest conservation genetics: principles and practice. CSIRO Publishing, Collingwood Vic, Australia, pp 215–224

    Google Scholar 

  • Andow DA, Zwahlen C (2006) Assessing environmental risks of transgenic plants. Ecol Lett 9:196–214

    Article  PubMed  CAS  Google Scholar 

  • Angevin F, Roturier C, Meynard JM, Klein EK (2003) Co-existence of GM, non-GM and organic maize crops in European agricultural landscapes: using MAPOD model to design necessary adjustments of farming practices. In: Proceedings of the first European conference on the co-existence of genetically modified crops with conventional and organic crops, Borupsgaard, 13–14 November 2003, pp 166–168

  • Arnaud J, Virad F, Delescluse M, Fuguen J (2003) Evidence for gene flow via seed dispersal from crop to wild relatives in Beta vulgaris (Chenopodiaceae): consequences for the release of genetically modified crop species with weedy lineages. Proc R Soc Lond B 270:1565–1571

    Article  Google Scholar 

  • Austerlitz F, Garnier-Gere PH (2003) Modeling the impact of colonisation on genetic diversity and differentiation of forest trees: interaction of life cycle, pollen flow and seed long-distance dispersal. Heredity 90:282–290

    Article  PubMed  CAS  Google Scholar 

  • Austerlitz F, Smouse PE (2001a) Two-generation analysis of pollen flow across a landscape. II. Relation between ϕ ft, pollen dispersal, and inter-female distance. Genetics 157:851–857

    PubMed  CAS  Google Scholar 

  • Austerlitz F, Smouse PE (2001b) Two-generation analysis of pollen flow across a landscape. III. Impact of within-population structure. Genet Res 78:271–280

    Article  PubMed  CAS  Google Scholar 

  • Austerlitz F, Smouse PE (2002) Two-generation analysis of pollen flow across a landscape. IV. Estimating the dispersal parameter. Genetics 161:355–363

    PubMed  Google Scholar 

  • Austerlitz F, Dick CW, Dutech C, Klein E, Oddou-Muratorio S, Smouse PE, Sork VL (2004) Using genetic markers to estimate the pollen dispersal curve. Mol Ecol 13:937–954

    Article  PubMed  Google Scholar 

  • Beckie HJ, Warwick SI, Nair H, Séguin-Swartz (2003) Gene flow in commercial fields of canola (Brassica napus). Ecol Appl 13:1276–1294

    Article  Google Scholar 

  • Bialozyt R, Ziegenhagen B, Petit RJ (2006) Contrasting effects of long distance seed dispersal on genetic diversity during range expansion. J Evol Biol 19:12–20

    Article  PubMed  CAS  Google Scholar 

  • Bohrer G, Nathan R, Volis S (2005) Effects of long-distance dispersal for metapopulation survival and genetic structure at ecological time and spatial scales. J Ecol 93:1029–1040

    Article  Google Scholar 

  • Burczyk J, Koralewski JE (2005) Parentage versus two-generation analyses for estimating pollen-mediated gene flow in plant populations. Mol Ecol 14:2525–2537

    Article  PubMed  CAS  Google Scholar 

  • Burczyk J, Adams WT, Shimizu JY (1996) Mating patterns and pollen dispersal in a natural knobcone pine (Pinus attenuata Lemmon) stand. Heredity 77:251–260

    Article  Google Scholar 

  • Burczyk J, Adams WT, Birkes DS, Chybicki IJ (2006) Using genetic markers to directly estimate gene flow and reproductive success parameters in plants based on naturally regenerated seedlings. Genetics 173:363–372

    Article  PubMed  CAS  Google Scholar 

  • Cain ML, Milligan BG, Strand AE (2000) Long-distance seed dispersal in plant populations. Am J Bot 87:1217–1227

    Article  PubMed  Google Scholar 

  • Clark J, Silman M, Kern R, Macklin E, HilleRisLambers J (1999) Seed dispersal near and far: patterns across temperate and tropical forests. Ecology 80:1475–1494

    Article  Google Scholar 

  • Colbach N, Clermont Dauphin C, Meynard JM (2001) GENESYS: a model on the influence of cropping system on gene escape from herbicide tolerant rape seed crops to volunteers–II. Genetic exchanges among volunteer and cropped populations in a small region. Agric Ecosys Environ 82:255–270

    Article  Google Scholar 

  • Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in forest trees. In: den Boer PJ, Gradwell GR (eds) Dynamics of populations. Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands, pp. 298–312

    Google Scholar 

  • Devaux C, Lavigne C, Falentin-Guyomarc’h H, Vautrin S, Lecomte J, Klein EK (2005) High diversity of oilseed rape pollen clouds over an agro-ecosystem indicates long-distance dispersal. Mol Ecol 14:2269–2280

    Article  PubMed  CAS  Google Scholar 

  • DiFazio SP, Slavov GT, Burczyk J, Leonardi S, Strauss SH (2004) Gene flow from tree plantations and implications for transgenic risk assessment. In: Walter C, Carson M (eds) Plantation forest biotechnology for the 21st century. Research Signpost, Kerala, India, pp 405–422

    Google Scholar 

  • Dow B, Ashley M (1996) Microsatellite analysis of seed dispersal and parentage of saplings in bur oak, Quercus macrocarpa. Mol Ecol 5:615–627

    Google Scholar 

  • Dyer RJ, Sork VL (2001) Pollen pool heterogeneity in shortleaf pine, Pinus echinata Mill. Mol Ecol 10:859–866

    Article  PubMed  CAS  Google Scholar 

  • Dyer RJ, Westfall RD, Sork VL, Smouse PE (2004) Two generation analysis of pollen flow across a landscape. V. A stepwise approach for extracting factors contributing to pollen structure. Heredity 92:204–211

    Article  PubMed  CAS  Google Scholar 

  • Eastham K, Sweet J (2002) Genetically modified organisms (GMOs): the significance of gene flow through pollen transfer. Environ Issue Report no. 86. European Environ Agency, pp 75

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Godoy JA, Jordano P (2001) Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites. Mol Ecol 10:2275–2283

    Article  PubMed  CAS  Google Scholar 

  • Gómez JS (2003) Spatial patterns in long-distance dispersal of Quercus ilex acorns by jays in a heterogeneous landscape. Ecography 26:573–584

    Article  Google Scholar 

  • González-Martínez SC, Gerber S, Cervera MT, Martínez-Zapater JM, Gil L, Alía R (2002) Seed gene flow and fine-scale structure in a Mediterranean pine (Pinus pinaster Ait.) using nuclear microsatellite markers. Theor Appl Genet 104:1290–1297

    Article  PubMed  CAS  Google Scholar 

  • González-Martínez SC, Robledo-Arnuncio JJ, Smouse PE (2005) The consequences and implications of introgression in the conservation of forest trees. In: de Vicente MC (ed) Gene flow and germplasm management issues in genetic resources. IPGRI, Rome, pp 17–23

    Google Scholar 

  • González-Martínez SC, Burczyk J, Nathan R, Gil L, Alía R (2006) Effective gene dispersal and mother-tree reproductive success in Mediterranean maritime pine (Pinus pinaster Aiton). Mol Ecol 15:4577–4588

    Google Scholar 

  • Grace SL, Hamrick JL, Platt WJ (2004) Estimation of seed dispersal in an old-growth population of longleaf pine (Pinus palustris) using maternity exclusion analysis. Castanea 69:207–215

    Article  Google Scholar 

  • Grivet D, Smouse PE, Sork VL (2005) A new approach to the study of seed dispersal: a novel approach to an old problem. Mol Ecol 14:3585–3595

    Article  PubMed  Google Scholar 

  • Grivet D, Sork VL, Smouse PE (2006) Spatial genetic pattern of dispersed seedlings in the California valley oak. In: Population genetics and genomics of forest trees. from gene function to evolutionary dynamics and conservation. Prog. Joint IUFRO Conf., Alcalá de Henares, Spain, p. I-SIII.4

  • Haygood R, Ives AR, Andow DA (2004) Population genetics of transgene containment. Ecol Lett 7:213–220

    Article  Google Scholar 

  • Hirschhorn JN, Daly MJ (2005) Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6:95–108

    Article  PubMed  CAS  Google Scholar 

  • Irwin AJ, Hamrick JL, Godt MJW, Smouse PE (2003) A multi-year estimate of the effective pollen donor pool for Albizia julibrissin. Heredity 90:187–194

    Article  PubMed  CAS  Google Scholar 

  • Isagi Y, Kanazashi T, Suzuki W, Tanaka H, Abe T (2000) Microsatellite analysis of the regeneration process of Magnolia obovata Thunb. Heredity 84:143–151

    Article  PubMed  CAS  Google Scholar 

  • Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528

    Article  Google Scholar 

  • Jing ZP, Gallardo F, Pascual MB, Sampalo R, Romero J, Torres de Navarra A, Cánovas DM (2004) Improved growth in a field trial of transgenic hybrid poplar overexpressing glutamine synthetase. New Phytol 164:137–145

    Article  CAS  Google Scholar 

  • Jones AG, Ardren WR (2003) Methods of parentage analysis in natural populations. Mol Ecol 12:2511–2523

    Article  PubMed  CAS  Google Scholar 

  • Jones FA, Chen J, Weng GJ, Hubbell SP (2005) A genetic evaluation of seed dispersal in the Neotropical tree Jacaranda copaia (Bignoniaceae). Am Nat 166:543–555

    Article  PubMed  CAS  Google Scholar 

  • Kelly CK, Bowler MG, Breden F, Fenner M, Poppy GM (2005) An analytical model assessing the potential threat to natural habitats from insect resistance transgenes. Proc Roy Soc Lond B 272:1759–1767

    Article  Google Scholar 

  • Klein EK, Lavigne C, Picault H, Renard M, Gouyon PH (2006) Pollen dispersal of oilseed rape: estimation of the dispersal function and effects of field dimension. J Appl Ecol 43:141–151

    Article  Google Scholar 

  • Kwok PY (2001) Methods for genotyping single nucleotide polymorphism. Ann Rev Genom Human Genet 2:235–258

    Article  CAS  Google Scholar 

  • LeCorre V, Machon N, Petit RJ, Kremer A (1997) Colonization with long-distance seed dispersal and genetic structure of maternally inherited genes in forest trees: a simulation study. Genet Res 69:117–125

    Article  Google Scholar 

  • Levey DJ, Sargent S (2000) A simple method for tracking vertebrate-dispersed seeds. Ecology 81:267–274

    Google Scholar 

  • Linacre NA, Ades PK (2004) Estimating isolation distances for genetically modified trees in plantation forestry. Ecol Model 179:247–257

    Article  Google Scholar 

  • Meagher TR, Thompson EA (1987) Analysis of paternity for naturally established seedlings of Chamaelirium luteum. Ecology 68:803–812

    Article  Google Scholar 

  • Meagher T, Belanger F, Day P (2003) Using empirical data to model transgene dispersal. Phil Trans R Soc Lond B 358:1157–1162

    Article  CAS  Google Scholar 

  • Messeguer J (2003) Gene flow assessment in transgenic plants. Plant Cell Tissue Organ Cult 73:201–212

    Article  CAS  Google Scholar 

  • Nakanishi A, Tomaru N, Yoshimaru H, Manabe T, Yamamoto S (2005) Interannual genetic heterogeneity of pollen pools accepted by Quercus salicina individuals. Mol Ecol 14:4469–4478

    Article  PubMed  CAS  Google Scholar 

  • Nathan R, Casagrandi R (2004) A simple mechanistic model of seed dispersal, predation and plant establishment: Janzen–Connell and beyond. J Ecol 92:733–746

    Article  Google Scholar 

  • Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285

    Article  PubMed  Google Scholar 

  • Nathan R, Perry G, Cronin JT, Strand AE, Cain ML (2003) Methods for estimating long-distance dispersal. Oikos 103:262–273

    Article  Google Scholar 

  • Oddou-Muratorio S, Klein EK, Austerlitz F (2005) Pollen flow in the wildservice tree, Sorbus torminalis (L.) Crantz. II. Pollen dispersal and heterogeneity in mating success inferred from parent-offspring analysis. Mol Ecol 14:4441–4452

    Article  PubMed  CAS  Google Scholar 

  • Petit RJ, Brewer S, Bordacs S et al (2002a) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. For Ecol Manag 156:49–74

    Article  Google Scholar 

  • Petit RJ, Csaikl UM, Bordacs S et al (2002b) Chloroplast DNA variation in European white oak phylogeography and patterns of diversity based on data from over 2600 populations. For Ecol Manag 156:5–26

    Article  Google Scholar 

  • Potts BM, Barbour RC, Hingston AB, Vaillancourt RE (2003) Genetic pollution of native eucalypt gene pools-identifying the risks. Am J Bot 51:1–25

    Article  Google Scholar 

  • Rieger MA, Lamond M, Preston C, Powles SB, Roush RT (2002) Pollen-mediated movement of herbicide resistance between commercial canola fields. Science 296:2386–2388

    Article  PubMed  CAS  Google Scholar 

  • Rieseberg LH, Burke JM (2001) The biological reality of species: gene flow, selection, and collective evolution. Taxon 50:47–67

    Article  Google Scholar 

  • Robledo-Arnuncio JJ, Smouse PE, Gil L, Alía R (2004) Pollen movement under alternative silvicultural practices in native populations of Scots pine (Pinus sylvestris L.) in central Spain. For Ecol Manag 197:245–255

    Article  Google Scholar 

  • Robledo-Arnuncio JJ, Austerlitz F, Smouse PE (2006) A new indirect method of estimating the pollen dispersal curve, independently of effective density. Genetics 173:1–14

    Article  CAS  Google Scholar 

  • Saeglitz C, Pohl M, Bartsch D (2000) Monitoring gene flow in transgenic sugar beet using cytoplasmic male-sterile bait plant. Mol Ecol 9:2035–2040

    Article  PubMed  CAS  Google Scholar 

  • Sato T, Isagi Y, Sakio H, Osumi K, Goto S (2006) Effect of gene flow on spatial genetic structure in the riparian canopy tree Cercidiphyllum japonicum revealed by microsatellite analysis. Heredity 96:79–84

    PubMed  CAS  Google Scholar 

  • Schmidtling RC (2001) Southern pine seed sources. USDA, GTR SRS-44, NC

  • Schnabel A, Nason JD, Hamrick JL (1998) Understanding the population genetic structure of Gleditsia triacanthos L: seed dispersal and variation in female reproductive success. Mol Ecol 7:819–832

    Article  Google Scholar 

  • Slavov GT, DiFazio SP, Strauss SH (2002) Gene flow in forest trees: from empirical estimates to transgenic risk assessment. In: Ecological and agronomic consequences of gene flow from transgenic crops to wild relatives, meeting proceedings. Ohio State University, Columbus, pp 106–126

  • Smouse PE, Robledo-Arnuncio JJ (2005) Measuring the genetic structure of the pollen pool as the probability of paternal identity. Heredity 94:640–649

    Article  PubMed  CAS  Google Scholar 

  • Smouse PE, Sork VL (2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. For Ecol Manag 197:21–38

    Article  Google Scholar 

  • Smouse PE, Dyer RJ, Westfall RD, Sork VL (2001) Two-generation analysis of pollen flow across a landscape. I. Male gamete heterogeneity among females. Evolution 55:260–271

    PubMed  CAS  Google Scholar 

  • Smouse PE, Hamrick JL, Trapnell DW, Hamrick K, Robledo-Arnuncio JJ, Gonzales E (2005) Full-sib analysis of pollen flow and pollen structure in Guanacaste (Enterolobium cyclocarpum) in the Costa Rican dry tropical forest. Prog. 50th Meet. Western Forest Genet. Assoc. http://www.fsl.orst.edu/wfga/WFGA2005Abstracts.pdf

  • Sork VL, Smouse PE (2006) Genetic analysis of landscape connectivity in tree populations. Landscape Ecol 21:821–836

    Article  Google Scholar 

  • Sork VL, Nason J, Campbell DR, Fernandez JF (1999) Landscape approaches to historical and contemporary gene flow in plants. Trends Ecol Evol 14:219–224

    Article  PubMed  Google Scholar 

  • Sork VL, Davis F, Smouse PE, Apsit V, Dyer R, Fernandez JM, Kuhn B (2002) Pollen movement in declining populations of California valley oak, Quercus lobata: Where have all the fathers gone? Mol Ecol 11:1657–1668

    Article  PubMed  CAS  Google Scholar 

  • Sork VL, Smouse PE, Apsit VJ, Dyer RJ, Westfall RD (2005) A two-generation analysis of pollen structure in Missouri Ozark populations of flowering dogwood (Cornus florida, Cornaceae). Am J Bot 92:262–271

    CAS  Google Scholar 

  • Stewart C (2005) Monitoring the presence and expression of transgenes in living plants. Trends Plant Sci 10:390–396

    Article  PubMed  CAS  Google Scholar 

  • Stewart C, Halfhill M, Warwick S (2003) Transgene introgression from genetically modified crops to their wild relatives. Nature Rev Genetics 4:806–817

    Article  CAS  Google Scholar 

  • Streiff R, Ducousso A, Lexer C, Steinkellner H, Gloessl J, Kremer A (1999) Pollen dispersal inferred from paternity analysis in a mixed oak stand of Quercus robur L. and Q. petraea (Matt.) Liebl. Mol Ecol 8:831–841

    Article  Google Scholar 

  • Valbuena-Carabaña M, González-Martínez SC, Sork VL, Collada C, Soto A, Goicoechea PG, Gil L (2005) Gene flow and hybridization in a mixed oak forest (Quercus pyrenaica Willd. and Q. petraea (Matts.) Liebl.) in central Spain. Heredity 95:457–465

    Article  PubMed  CAS  Google Scholar 

  • van Frankenhuyzen K, Beardmore T (2004) Current status and environmental impact of transgenic forest trees. Can J For Res 34:1163–1180

    Article  Google Scholar 

  • Watrud LS, Lee EH, Fairbrother A, Burdick C, Reichman JR, Bollman M, Storm M, King G, Van de Water P (2004) Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. Proc Natl Acad Sci U S A 101:14533–14538

    Article  PubMed  CAS  Google Scholar 

  • Williams C, Davis B (2005) Rate of transgene spread via long-distance seed dispersal in Pinus taeda. For Ecol Manag 217:95–102

    Article  Google Scholar 

  • Williams CG, LaDeau SL, Oren R, Katul GG (2006) Modeling seed dispersal distances: implications for transgenic Pinus taeda. Ecol Appl 16:117–124

    Article  PubMed  Google Scholar 

  • Ziegenhagen B, Liepelt S, Kuhlenkamp V, Fladung M (2003) Molecular identification of individual oak and fir trees from maternal tissues of their fruits or seeds. Trees 17:345–350

    CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Fred Austerlitz, Eva Gonzales, Victoria Sork, B Wang, and a trio of anonymous reviewers for many helpful comments on the manuscript. PES was supported by USDA/NJAES-17111 and by NSF-DEB-0211430 and NSF-DEB-0514956; JJR-A was supported by a postdoctoral fellowship from the Spanish Secretaría de Estado de Educación y Universidades, financed in part by the European Social Fund; SCG-M was supported by the ‘Ramón y Cajal’ fellowship RC02-2941 and by AGL2005-07440-C02-01 grant (Ministerio de Educación y Ciencia, Spain).

Author information

Authors and Affiliations

  1. Department Ecology, Evolution and Natural Resources, Cook College, Rutgers University, Room 152 ENRS Building, 14 College Farm Road, New Brunswick, NJ, 08901, USA

    Peter E. Smouse & Juan J. Robledo-Arnuncio

  2. Laboratoire Génétique et Environnement, Université de Montpellier II, Institut des Sciences de l’Evolution, CC065, Place Eugène Bataillon, 34095, Montpellier Cedex 05, France

    Juan J. Robledo-Arnuncio

  3. Departamento de Sistemas y Recursos Forestales, CIFOR-INIA, Carretera de La Coruña km 7.5, 28040, Madrid, Spain

    Santiago C. González-Martínez

Authors
  1. Peter E. Smouse
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan J. Robledo-Arnuncio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Santiago C. González-Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter E. Smouse.

Additional information

Communicated by Ronald Sederoff

Institute of Forest Biotechnology conference on Ecological Risks Associated with the Products of Forest Biotechnology

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smouse, P.E., Robledo-Arnuncio, J.J. & González-Martínez, S.C. Implications of natural propagule flow for containment of genetically modified forest trees. Tree Genetics & Genomes 3, 141–152 (2007). https://doi.org/10.1007/s11295-006-0075-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11295-006-0075-8

Keywords

Search

Navigation