Tree Genetics & Genomes

, Volume 3, Issue 2, pp 141–152 | Cite as

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

  • Peter E. Smouse
  • Juan J. Robledo-Arnuncio
  • Santiago C. González-Martínez
Original Paper


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.


Forest trees Gene flow GMO escapes Monitoring Transgenic risks 


  1. Adams WT, Birkes DS (1989) Mating patterns in seed orchards. In: Proceedings of the 20th southern forest tree improvement conference, Charleston, pp. 75–86Google Scholar
  2. 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 157–172Google Scholar
  3. 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 215–224Google Scholar
  4. Andow DA, Zwahlen C (2006) Assessing environmental risks of transgenic plants. Ecol Lett 9:196–214PubMedCrossRefGoogle Scholar
  5. 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 166–168Google Scholar
  6. 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 270:1565–1571CrossRefGoogle Scholar
  7. 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 90:282–290PubMedCrossRefGoogle Scholar
  8. 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 157:851–857PubMedGoogle Scholar
  9. Austerlitz F, Smouse PE (2001b) Two-generation analysis of pollen flow across a landscape. III. Impact of within-population structure. Genet Res 78:271–280PubMedCrossRefGoogle Scholar
  10. Austerlitz F, Smouse PE (2002) Two-generation analysis of pollen flow across a landscape. IV. Estimating the dispersal parameter. Genetics 161:355–363PubMedGoogle Scholar
  11. 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 13:937–954PubMedCrossRefGoogle Scholar
  12. Beckie HJ, Warwick SI, Nair H, Séguin-Swartz (2003) Gene flow in commercial fields of canola (Brassica napus). Ecol Appl 13:1276–1294CrossRefGoogle Scholar
  13. Bialozyt R, Ziegenhagen B, Petit RJ (2006) Contrasting effects of long distance seed dispersal on genetic diversity during range expansion. J Evol Biol 19:12–20PubMedCrossRefGoogle Scholar
  14. 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 93:1029–1040CrossRefGoogle Scholar
  15. Burczyk J, Koralewski JE (2005) Parentage versus two-generation analyses for estimating pollen-mediated gene flow in plant populations. Mol Ecol 14:2525–2537PubMedCrossRefGoogle Scholar
  16. Burczyk J, Adams WT, Shimizu JY (1996) Mating patterns and pollen dispersal in a natural knobcone pine (Pinus attenuata Lemmon) stand. Heredity 77:251–260CrossRefGoogle Scholar
  17. 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 173:363–372PubMedCrossRefGoogle Scholar
  18. Cain ML, Milligan BG, Strand AE (2000) Long-distance seed dispersal in plant populations. Am J Bot 87:1217–1227PubMedCrossRefGoogle Scholar
  19. Clark J, Silman M, Kern R, Macklin E, HilleRisLambers J (1999) Seed dispersal near and far: patterns across temperate and tropical forests. Ecology 80:1475–1494CrossRefGoogle Scholar
  20. 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 82:255–270CrossRefGoogle Scholar
  21. 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. 298–312Google Scholar
  22. 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 14:2269–2280PubMedCrossRefGoogle Scholar
  23. 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 405–422Google Scholar
  24. Dow B, Ashley M (1996) Microsatellite analysis of seed dispersal and parentage of saplings in bur oak, Quercus macrocarpa. Mol Ecol 5:615–627Google Scholar
  25. Dyer RJ, Sork VL (2001) Pollen pool heterogeneity in shortleaf pine, Pinus echinata Mill. Mol Ecol 10:859–866PubMedCrossRefGoogle Scholar
  26. 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 92:204–211PubMedCrossRefGoogle Scholar
  27. 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 75Google Scholar
  28. 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 131:479–491PubMedGoogle Scholar
  29. Godoy JA, Jordano P (2001) Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites. Mol Ecol 10:2275–2283PubMedCrossRefGoogle Scholar
  30. Gómez JS (2003) Spatial patterns in long-distance dispersal of Quercus ilex acorns by jays in a heterogeneous landscape. Ecography 26:573–584CrossRefGoogle Scholar
  31. 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 104:1290–1297PubMedCrossRefGoogle Scholar
  32. 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 17–23Google Scholar
  33. 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 15:4577–4588Google Scholar
  34. 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 69:207–215CrossRefGoogle Scholar
  35. 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 14:3585–3595PubMedCrossRefGoogle Scholar
  36. 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.4Google Scholar
  37. Haygood R, Ives AR, Andow DA (2004) Population genetics of transgene containment. Ecol Lett 7:213–220CrossRefGoogle Scholar
  38. Hirschhorn JN, Daly MJ (2005) Genome-wide association studies for common diseases and complex traits. Nat Rev Genet 6:95–108PubMedCrossRefGoogle Scholar
  39. Irwin AJ, Hamrick JL, Godt MJW, Smouse PE (2003) A multi-year estimate of the effective pollen donor pool for Albizia julibrissin. Heredity 90:187–194PubMedCrossRefGoogle Scholar
  40. Isagi Y, Kanazashi T, Suzuki W, Tanaka H, Abe T (2000) Microsatellite analysis of the regeneration process of Magnolia obovata Thunb. Heredity 84:143–151PubMedCrossRefGoogle Scholar
  41. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528CrossRefGoogle Scholar
  42. 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 164:137–145CrossRefGoogle Scholar
  43. Jones AG, Ardren WR (2003) Methods of parentage analysis in natural populations. Mol Ecol 12:2511–2523PubMedCrossRefGoogle Scholar
  44. Jones FA, Chen J, Weng GJ, Hubbell SP (2005) A genetic evaluation of seed dispersal in the Neotropical tree Jacaranda copaia (Bignoniaceae). Am Nat 166:543–555PubMedCrossRefGoogle Scholar
  45. 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 272:1759–1767CrossRefGoogle Scholar
  46. 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 43:141–151CrossRefGoogle Scholar
  47. Kwok PY (2001) Methods for genotyping single nucleotide polymorphism. Ann Rev Genom Human Genet 2:235–258CrossRefGoogle Scholar
  48. 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 69:117–125CrossRefGoogle Scholar
  49. Levey DJ, Sargent S (2000) A simple method for tracking vertebrate-dispersed seeds. Ecology 81:267–274Google Scholar
  50. Linacre NA, Ades PK (2004) Estimating isolation distances for genetically modified trees in plantation forestry. Ecol Model 179:247–257CrossRefGoogle Scholar
  51. Meagher TR, Thompson EA (1987) Analysis of paternity for naturally established seedlings of Chamaelirium luteum. Ecology 68:803–812CrossRefGoogle Scholar
  52. Meagher T, Belanger F, Day P (2003) Using empirical data to model transgene dispersal. Phil Trans R Soc Lond B 358:1157–1162CrossRefGoogle Scholar
  53. Messeguer J (2003) Gene flow assessment in transgenic plants. Plant Cell Tissue Organ Cult 73:201–212CrossRefGoogle Scholar
  54. Nakanishi A, Tomaru N, Yoshimaru H, Manabe T, Yamamoto S (2005) Interannual genetic heterogeneity of pollen pools accepted by Quercus salicina individuals. Mol Ecol 14:4469–4478PubMedCrossRefGoogle Scholar
  55. Nathan R, Casagrandi R (2004) A simple mechanistic model of seed dispersal, predation and plant establishment: Janzen–Connell and beyond. J Ecol 92:733–746CrossRefGoogle Scholar
  56. Nathan R, Muller-Landau HC (2000) Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol Evol 15:278–285PubMedCrossRefGoogle Scholar
  57. Nathan R, Perry G, Cronin JT, Strand AE, Cain ML (2003) Methods for estimating long-distance dispersal. Oikos 103:262–273CrossRefGoogle Scholar
  58. 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 14:4441–4452PubMedCrossRefGoogle Scholar
  59. 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 156:49–74CrossRefGoogle Scholar
  60. 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 156:5–26CrossRefGoogle Scholar
  61. Potts BM, Barbour RC, Hingston AB, Vaillancourt RE (2003) Genetic pollution of native eucalypt gene pools-identifying the risks. Am J Bot 51:1–25CrossRefGoogle Scholar
  62. Rieger MA, Lamond M, Preston C, Powles SB, Roush RT (2002) Pollen-mediated movement of herbicide resistance between commercial canola fields. Science 296:2386–2388PubMedCrossRefGoogle Scholar
  63. Rieseberg LH, Burke JM (2001) The biological reality of species: gene flow, selection, and collective evolution. Taxon 50:47–67CrossRefGoogle Scholar
  64. 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 197:245–255CrossRefGoogle Scholar
  65. Robledo-Arnuncio JJ, Austerlitz F, Smouse PE (2006) A new indirect method of estimating the pollen dispersal curve, independently of effective density. Genetics 173:1–14CrossRefGoogle Scholar
  66. Saeglitz C, Pohl M, Bartsch D (2000) Monitoring gene flow in transgenic sugar beet using cytoplasmic male-sterile bait plant. Mol Ecol 9:2035–2040PubMedCrossRefGoogle Scholar
  67. 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 96:79–84PubMedGoogle Scholar
  68. Schmidtling RC (2001) Southern pine seed sources. USDA, GTR SRS-44, NCGoogle Scholar
  69. 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 7:819–832CrossRefGoogle Scholar
  70. 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 106–126Google Scholar
  71. Smouse PE, Robledo-Arnuncio JJ (2005) Measuring the genetic structure of the pollen pool as the probability of paternal identity. Heredity 94:640–649PubMedCrossRefGoogle Scholar
  72. Smouse PE, Sork VL (2004) Measuring pollen flow in forest trees: an exposition of alternative approaches. For Ecol Manag 197:21–38CrossRefGoogle Scholar
  73. 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 55:260–271PubMedGoogle Scholar
  74. 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.
  75. Sork VL, Smouse PE (2006) Genetic analysis of landscape connectivity in tree populations. Landscape Ecol 21:821–836CrossRefGoogle Scholar
  76. Sork VL, Nason J, Campbell DR, Fernandez JF (1999) Landscape approaches to historical and contemporary gene flow in plants. Trends Ecol Evol 14:219–224PubMedCrossRefGoogle Scholar
  77. 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 11:1657–1668PubMedCrossRefGoogle Scholar
  78. 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 92:262–271Google Scholar
  79. Stewart C (2005) Monitoring the presence and expression of transgenes in living plants. Trends Plant Sci 10:390–396PubMedCrossRefGoogle Scholar
  80. Stewart C, Halfhill M, Warwick S (2003) Transgene introgression from genetically modified crops to their wild relatives. Nature Rev Genetics 4:806–817CrossRefGoogle Scholar
  81. 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 8:831–841CrossRefGoogle Scholar
  82. 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 95:457–465PubMedCrossRefGoogle Scholar
  83. van Frankenhuyzen K, Beardmore T (2004) Current status and environmental impact of transgenic forest trees. Can J For Res 34:1163–1180CrossRefGoogle Scholar
  84. 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 101:14533–14538PubMedCrossRefGoogle Scholar
  85. Williams C, Davis B (2005) Rate of transgene spread via long-distance seed dispersal in Pinus taeda. For Ecol Manag 217:95–102CrossRefGoogle Scholar
  86. Williams CG, LaDeau SL, Oren R, Katul GG (2006) Modeling seed dispersal distances: implications for transgenic Pinus taeda. Ecol Appl 16:117–124PubMedCrossRefGoogle Scholar
  87. 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 17:345–350Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Peter E. Smouse
    • 1
  • Juan J. Robledo-Arnuncio
    • 1
    • 2
  • Santiago C. González-Martínez
    • 3
  1. 1.Department Ecology, Evolution and Natural Resources, Cook CollegeRutgers UniversityNew BrunswickUSA
  2. 2.Laboratoire Génétique et Environnement, Université de Montpellier IIInstitut des Sciences de l’EvolutionMontpellier Cedex 05France
  3. 3.Departamento de Sistemas y Recursos ForestalesCIFOR-INIAMadridSpain

Personalised recommendations