Advertisement

Biological Invasions

, 11:1093 | Cite as

Hybridization and the evolution of invasiveness in plants and other organisms

  • Kristina A. SchierenbeckEmail author
  • Norman C. Ellstrand
Original Paper

Abstract

Less than a decade ago, we proposed that hybridization could serve as a stimulus for the evolution of invasiveness in plants (Ellstrand and Schierenbeck Proc Nat Acad Sci USA 97:7043–7050, 2000). A substantial amount of research has taken place on that topic since the publication of that paper, stimulating the symposium that makes up this special issue. Here we present an update of this emergent field, based both on the papers in this volume and on the relevant literature. We reevaluate the lists that we presented in our earlier paper of reports in which hybridization has preceded the evolution of invasiveness. We discard a few cases that were found to be in error, published only as abstracts, or based on personal communication. Then we augment the list from examples in this volume and a supplementary literature search. Despite the omissions, the total number of cases has increased. Many have been strengthened. We add a list of cases in which there has been evidence that intra-taxon hybridization has preceded the evolution of invasiveness. We also provide a number of examples from organisms other than plants. We consider how our examples suggest mechanisms whereby hybridization may act to stimulate the evolution of invasiveness. Hybridization does not represent the only evolutionary pathway to invasiveness, but it is one that can explain why the appearance of invasiveness often involves a long lag time and/or multiple introductions of exotics.

Keywords

Evolution Gene flow Hybridization Invasive plants Weeds 

Notes

Acknowledgments

This work was supported by funding from National Science Foundation Grants (9973734 and 9322795) to K.A.S. and from a University of California Competitive grant (1997-980069), an Environmental Protection Agency grant (R-826102-01-0), a USDA NRI CSREES Grant (2003-35320-13559), and a National Science Foundation Biocomplexity Grant (DEB-0409984) to N.C.E. This work also benefited from conversations with participants from the NSF-Research Collaboration Network grant to Ruth Hufbauer and Mark Torchin (DEB-0541673).

References

  1. Abbott RJ, Milne RI (1995) Origins and evolutionary effects of invasive weeds. In: BCPC symposium proceedings: weeds in a changing world, vol 64, pp 53–64Google Scholar
  2. Abbott RJ, James JK, Irwin JA, Comes HP (2000) Hybrid origin of the Oxford ragwort, Senecio squalidus L. Watsonia 23:123–138Google Scholar
  3. Abbott RJ, James JK, Milne RI, Gillies ACM (2003) Plant introductions, hybridization, and gene flow. Philos Trans R Soc Lond B 358:1123–1132CrossRefGoogle Scholar
  4. Abbott RJ, Brennan AC, James JK, Forbes DG, Hegarty MJ, Hiscock SJ (2008) Recent hybrid origin and invasion of the British Isles by aself-incompatible species, Oxford ragwort (Senecio squalidus L., Asteraceae). Biol Invasions (this issue). doi: 10.1007/s10530-008-9382-3
  5. Aïnouche M, Bayer RJ, Gourret JP, Defontaine A, Misset MT (1999) The allotetraploid invasive weed Bromus hordaceus L. (Poaceae): genetic diversity, origin and molecular evolution. Folia Geobot 34:405–419CrossRefGoogle Scholar
  6. Aïnouche M, Fortune PM, Salmon A, Parisod C, Grandbastien M-A, Fukunaga K, Ricou M, Misset M-T (2008) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biol Invasions (this issue). doi: 10.1007/s10530-008-9383-2
  7. Anderson E (1948) Hybridization of the habitat. Evolution 2:1–9CrossRefGoogle Scholar
  8. Anderson NO, Galatowitsch SM, Gomez N (2006) Selection strategies to reduce invasive potential in introduced plants. Euphytica 148:203–216CrossRefGoogle Scholar
  9. Ayres DR, Smith DL, Zaremba K, Klohr S, Strong DR (2004) Spread of exotic cordgrasses and hybrids (Spartina sp.) in the tidal marshes of San Francisco Bay. Biol Invasions 6:221–231CrossRefGoogle Scholar
  10. Ayres DR, Ryan FJ, Grotkopp E, Bailey J, Gaskin J (2008) Tumbleweed (Salsola, section Kali) species and speciation in California. Biol Invasions (this issue). doi: 10.1007/s10530-008-9380-5
  11. Bailey JP, Bímová K, Mandák B (2008) Asexual spread versus sexual reproduction and evolution in Japanese Knotweed s.l. sets the stage for the “Battle of the Clones”. Biol Invasions (this issue). doi: 10.1007/s10530-008-9381-4
  12. Baskin CC, Baskin JM (1998) Seeds: ecology, biogeography and evolution of dormancy and germination. Academic Press, San DiegoGoogle Scholar
  13. Bleeker W (2003) Hybridization and Rorippa austriaca (Brassicaceae) invasion in Germany. Mol Ecol 12:1831–1841PubMedCrossRefGoogle Scholar
  14. Bleeker W, Huthman M, Hurka H (1999) Evolution of hybrid taxa in Nasturtium R. Br. (Brassicaceae). Folia Geobot Phytotaxon 34:421–433CrossRefGoogle Scholar
  15. Blossey B, Nötzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889CrossRefGoogle Scholar
  16. Brasier CM, Cooke DEL, Duncan JM (1999) Origin of a new Phytophthora pathogen through interspecific hybridization. Proc Natl Acad Sci USA 96:5878–5883PubMedCrossRefGoogle Scholar
  17. Brusati ED, Grosholz ED (2006) Native and introduced ecosystem engineers produce contrasting effects on estuarine infaunal communities. Biol Invasions 8:683–695CrossRefGoogle Scholar
  18. Burger JC, Lee S, Ellstrand NC (2006) Origin and genetic structure of feral rye in the western United States. Mol Ecol 15:2527–2539PubMedCrossRefGoogle Scholar
  19. Campbell CS, Wojciechowski MF, Baldwin BG, Alice LA, Donoghue MJ (1997) Persistent nuclear ribosomal DNA sequence polymorphism in the Amelanchier agamic complex (Rosaceae). Mol Biol Evol 14:81–90PubMedGoogle Scholar
  20. Cleland RE (1972) Oenothera. Cytogenetics and evolution. Academic Press, LondonGoogle Scholar
  21. Coart E, Vekemans X, Smulders MJM et al (2003) Genetic variation in the endangered wild apple (Malus sylvestris (L.) Mill.) in Belgium as revealed by amplified fragment length polymorphism and microsatellite markers. Mol Ecol 12:845–857PubMedCrossRefGoogle Scholar
  22. Cronn R, Wendel JF (2004) Cryptic trysts, genomic mergers, and plant speciation. New Phytol 161:133–142CrossRefGoogle Scholar
  23. Culley T, Hardiman N (2008) The role of intraspecific hybridization in the evolution of invasiveness: a case study of the ornamental pear tree Pyrus calleryana. Biol Invasions (this issue). doi: 10.1007/s10530-008-9386-z
  24. Dekker J (1997) Weed diversity and weed management. Weed Sci 45:357–363Google Scholar
  25. Dekker J (1999) Soil weed seed banks and weed management. J Crop Prod 2:139–166CrossRefGoogle Scholar
  26. deWalt SJ, Hamrick JL (2004) Genetic variation of introduced Hawaiian and native Costa Rican populations of an invasive tropical shrub, Clidemia hirta (Melastomataceae). Am J Bot 91:1155–1163CrossRefGoogle Scholar
  27. Dukes JS, Mooney HA (2004) Disruption of ecosystem process in western North America by invasive species. Rev Chil Hist Hat 77:411–437Google Scholar
  28. Durand C, Manuel M, Boudouresque CF, Meinesz A, Verlaque M, Le Parco Y (2002) Molecular data suggest a hybrid origin for the invasive Caulerpa racemosa (Caulerpales, Chlorophyta) in the Mediterranean Sea. J Evol Biol 15:122–133CrossRefGoogle Scholar
  29. Durka W, Bossdorf O, Prati D, Auge H (2005) Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol Ecol 14:1697–1706PubMedCrossRefGoogle Scholar
  30. Ellstrand NC, Schierenbeck K (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Nat Acad Sci USA 97:7043–7050PubMedCrossRefGoogle Scholar
  31. Ellstrand NC, Whitkus R, Rieseberg LH (1996) Distribution of spontaneous plant hybrids. Proc Nat Acad Sci 93:5090–5093PubMedCrossRefGoogle Scholar
  32. Ennos RA (1994) Estimating the relative rates of pollen and seed migration. Heredity 72:250–259CrossRefGoogle Scholar
  33. Facon B, Jarne P, Pointier JP, David P (2005) Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance. J Evol Biol 18:524–535PubMedCrossRefGoogle Scholar
  34. Figueroa ME, Castillo JM, Redondo S, Luque T, Castellanos EM, Nieva FJ, Luque CJ, Rubio-Casal AE, Davy AJ (2003) Facilitated invasion by hybridization of Sarcocornia species in a salt-marsh succession. J Ecol 91:616–626CrossRefGoogle Scholar
  35. Gallagher KG, Schierenbeck KA, D’Antonio CM (1997) Hybridization and introgression in Carpobrotus spp. (Aizoaceae) in California. II. Allozyme evidence. Am J Bot 84:905–911CrossRefGoogle Scholar
  36. Gaskin JF, Kazmer DJ (2008) Introgression between saltcedars (Tamarix chinensis and T. ramosissima) in the USA invasion. Biol Invasions (this issue). doi: 10.1007/s10530-008-9384-1
  37. Gaskin JG, Schaal BA (2002) Hybrid Tamarix widespread in U.S. invasion and undetected in native Asian range. Proc Nat Acad Sci USA 99:11256–11259PubMedCrossRefGoogle Scholar
  38. Grant V (1981) Plant speciation. Columbia University Press, New YorkGoogle Scholar
  39. Gray AJ, Marshall DF, Raybould AF (1991) A century of evolution in Spartina anglica. Adv Ecol Res 21:1–62CrossRefGoogle Scholar
  40. Gressel J (2005) Crop ferality and volunteerism. CRC Press, Boca RatonGoogle Scholar
  41. Hall RJ, Hastings A, Ayres DR (2006) Explaining the explosion: modelling hybrid invasions. Proc R Soc Lond B 273:1385–1389CrossRefGoogle Scholar
  42. Hawkes JG (1990) The potato: evolution, biodiversity and genetic resources. Bellhaven Press, LondonGoogle Scholar
  43. Hegde SG, Nason JD, Clegg J, Ellstrand NC (2006) The evolution of California’s wild radish has resulted in the extinction of its progenitors. Evolution 60:1187–1197PubMedGoogle Scholar
  44. Houghton-Thompson J, Prince HH, Smith JJ, Hancock JH (2005) Evidence of hybridization between Lythrum salicaria (purple loosestrife) and L. alatum (winged loosestrife) in North America. Ann Bot 96:877–885PubMedCrossRefGoogle Scholar
  45. Koehler-Santos P, Lorenz-Lemke AP, Salzano FM, Freitas LB (2006) Ecological-evolutionary relationships in Passiflora alata from Rio Grande do Sul, Brazil. Braz J Biol 66:809–816PubMedCrossRefGoogle Scholar
  46. Kolbe JJ, Glor RE, Rodríguez Schettino L, Chamizo Lara A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181PubMedCrossRefGoogle Scholar
  47. Kuehn MM, Minor JE, White BN (1999) An examination of hybridization between the cattail species Typha latifolia and Typha angustifolia using random amplified polymorphic DNA and chloroplast DNA markers. Mol Ecol 8:1981–1990PubMedCrossRefGoogle Scholar
  48. Lambrinos JG (2004) How interactions between ecology and evolution influence cotemporary invasion dynamics. Ecology 85:2061–2070CrossRefGoogle Scholar
  49. Latta RG, Gardner KM, Johansen-Morris AD (2007) Hybridization, recombination, and the genetic basis of fitness variation across environments in Avena barbata. Genetica 12:16–67Google Scholar
  50. Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888PubMedCrossRefGoogle Scholar
  51. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  52. Levin DA (1979) The nature of plant species. Science 204:381–384PubMedCrossRefGoogle Scholar
  53. Levine JM, Vila M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond Ser B 270:775–781CrossRefGoogle Scholar
  54. Lihova J, Tribsch A, Marhold K (2003) The Cardamine pratensis (Brassicaceae) group in the Iberian Peninsula: taxonomy, polyploidy and distribution. Taxon 52:783–801CrossRefGoogle Scholar
  55. Marchais L (1994) Wild pearl millet population (Pennisetum glaucum, Poaceae) integrity in agricultural Sahelian areas. An example from Keita (Niger). Plant Syst Evol 189:233–245CrossRefGoogle Scholar
  56. McCauley DE (1997) The relative contributions of seed and pollen movement to the local genetic structure of Silene alba. J Hered 88:257–263Google Scholar
  57. Milne RI, Abbott RJ (2000) Origin and evolution of invasive naturalised material of Rhododendron ponticum L. in the British Isles. Mol Ecol 9:541–556PubMedCrossRefGoogle Scholar
  58. Milne RI, Abbott RJ (2004) Geographic origin and taxonomic status of the invasive privet, Ligustrum robustum in the Mascarene Islands. Heredity 92:78–87PubMedCrossRefGoogle Scholar
  59. Moody ML, Les DH (2002) Evidence of hybridity in invasive watermilfoil (Myriophyllum) populations. Proc Nat Acad Sci USA 23:14867–14871CrossRefGoogle Scholar
  60. Neuffer B, Auge H, Mesch H, Amarell U, Brandl R (1999) Spread of violets in polluted pine forests: morphological and molecular evidence for the ecological importance of interspecific hybridization. Mol Ecol 8:365–377Google Scholar
  61. Novak SJ, Soltis DE, Soltis PS (1991) Ownbey’s Tragopogons: 40 years later. Am J Bot 78:1586–1600CrossRefGoogle Scholar
  62. Nuber N, Gornik O, Lauc G, Bauer N, Žuljević A, Papeš D, Zoldoš V (2007) Genetic evidence for the identity of Caulerpa racemosa (Forsskål) J. Agardh (Caulerpales, Chlorophyta) in the Adriatic Sea. Eur J Phycol 42:113–120CrossRefGoogle Scholar
  63. O’Hanlon PC, Peakall R, Briese DT (1999) Amplified fragment length polymorphism (AFLP) reveals introgression in weedy Onopordum thistles: hybridization and invasion. Mol Ecol 8:1239–1246PubMedCrossRefGoogle Scholar
  64. Olden JD, Rooney TP (2006) On defining and quantifying biotic homogenization. Global Eco Biogeogr 15:113–120CrossRefGoogle Scholar
  65. Olden J, Poff NL, Douglas MR, Douglas ME, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24PubMedCrossRefGoogle Scholar
  66. Parker IM, Kareiva P (1994) Assessing the risk of invasion in genetically modified crops: an ecological perspective. In: Jones DD (ed) The biosafety results of field tests of genetically modified plants and microorganisms. University of California Division of Agriculture and Natural Resources, Oakland, pp 467–470Google Scholar
  67. Paterson AH, Schertz KF, Lin YR, Liu SC, Chang YL (1995) The weediness of wild plants: molecular analysis of genes influencing dispersal and persistence of johnsongrass, Sorghum halepense (L.) Pers. Proc Natl Acad Sci USA 92:6127–6131PubMedCrossRefGoogle Scholar
  68. Petit RJ (2004) Biological invasions at the gene level. Div Distrib 10:159–165CrossRefGoogle Scholar
  69. Pinto MA, Rubink WL, Patton JC, Coulson RN, Johnston JS (2005) Africanization in the United States: replacement of feral European honeybees (Apis mellifera L.) by an African hybrid swarm. Genetics 170:1653–1665PubMedCrossRefGoogle Scholar
  70. Purugganan MD (2000) The molecular population genetics of regulatory genes. Mol Ecol 9:1451–1461PubMedCrossRefGoogle Scholar
  71. Rieseberg LH, Ellstrand NC (1993) What can molecular and morphological markers tell us about plant hybridization? Crit Rev Pl Sci 12:213–241CrossRefGoogle Scholar
  72. Rieseberg LH, Carter R, Zona S (1990) Molecular tests of the hypothesized hybrid origin of two diploid Helianthus species. Evolution 44:1498–1511CrossRefGoogle Scholar
  73. Saltonstall K (2003) Microsatellite variation within and among North American lineages of Phragmites australis. Mol Ecol 12:1689–1702PubMedCrossRefGoogle Scholar
  74. Schierenbeck KA, Aïnouche ML (2005) Evolutionary consequences of plant invasions. In: Cadotte MW, McMahon SM, Fukami T (eds) Conceptual ecology and invasions biology: reciprocal approaches to nature. Kluwer Press, The Netherlands, pp 193–221Google Scholar
  75. Schierenbeck KA, Symonds VV, Gallagher KG, Bell J (2005) Genetic variation and phylogeographic analyses of two species of Carpobrotus and their hybrids in California. Mol Ecol 14:539–547PubMedCrossRefGoogle Scholar
  76. Sloop CM, Ayres DR, Strong DR (2008) The rapid evolution of self- fertility in Spartina hybrids (Spartina alterniflora x foliosa) invading San Francisco Bay, CA. Biol Invasions (this issue). doi: 10.1007/s10530-008-9385-0
  77. Slotta TAB, Rothhouse J, Horvath DP, Foley ME (2006) Genetic diversity of Cirsium arvense (Canada thistle) in North Dakota. Weed Sci 54:1080–1085CrossRefGoogle Scholar
  78. Smoot LM, Franke DD, McGillivary G, Actis LA (2002) Genomic analysis of the F3031 Brazilian purpuric fever clone of Haemophilus influenzae biogroup Aegyptius by PCR-based subtractive hybridization. Infect Immun 70:2694–2699PubMedCrossRefGoogle Scholar
  79. Stace CA (1975) Hybridization and the flora of the British Isles. Academic Press, LondonGoogle Scholar
  80. Stace CA (1991) New flora of the British Isles. Cambridge University Press, CambridgeGoogle Scholar
  81. Suarez AD, Tsutsui N (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360Google Scholar
  82. Sukopp U, Pohl M, Driessen S, Bartsch D (2005) Feral beets—with help from the maritime wild? In: Gressel J (ed) Crop ferality and volunteerism. Taylor & Francis, Boca Raton, pp 45–57Google Scholar
  83. Suneson CA, Rachie KO, Khush GS (1969) A dynamic population of weedy rye. Crop Sci 9:121–124Google Scholar
  84. Sweeney BW, Bott TL, Jackson JK, Kaplan LA, Newbold JD, Standley LJ, Hession WC, Horwitz RJ (2004) Riparian deforestation, stream narrowing, and loss of stream ecosystem services. Proc Nat Acad Sci USA 101:14132–14137PubMedCrossRefGoogle Scholar
  85. Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8:895–908CrossRefGoogle Scholar
  86. Taylor CM, Davis HG, Civille JC, Grevstad FS, Hastings A (2004) Consequences of an allee effect in the invasive of a Pacific estuary by Spartina alterniflora. Ecology 85:3254–3266CrossRefGoogle Scholar
  87. Urbanska KM, Hruka H, Landolt E, Neuffer B, Mummenhoff K (1997) Hybridization and evolution in Cardamine (Brassicaceae) at Urnerboden, Central Switzerland: Biosystematic and molecular evidence. Plant Syst Evol 204:233–256CrossRefGoogle Scholar
  88. Viard F, Bernard J, Desplanque B (2002) Crop-weed interaction in the Beta vulgaris complex at the local scale: allelic diversity and gene flow within sugar beet fields. Theor Appl Genet 104:688–697PubMedCrossRefGoogle Scholar
  89. Waterhouse B, Zeimer O (2002) On the brink: status of chromolaena odorata in Northern Australia. In: Zachariades C, Muniappan R, Strathie LW (eds) Proceedings of the fifth international workshop on biological control and management of chromolaena odorata. Durban, South Africa, pp 66–70, 23–25 October 2000 ARC-PPRIGoogle Scholar
  90. Whitney KD, Ahern JR, Campbell LG (2008). Hybridization-prone plant families do not generate more invasive species. Biol Invasions (this issue). doi: 10.1007/s10530-008-9390-3
  91. Williams DA, Overholt WA, Cuda JP, Hughes CR (2005) Chloroplast and microsatellite DNA diversities reveal the introduction history of Brazilian peppertree (Schinus terebinthifolius) in Florida. Mol Ecol 14:3643–3656PubMedCrossRefGoogle Scholar
  92. Wolfe LM, Blair AM, Penna BM (2007) Does intraspecific hybridization contribute to the evolution of invasiveness? An experimental test. Biol Invasions 9:1387–3547CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Kristina A. Schierenbeck
    • 1
    • 2
    Email author
  • Norman C. Ellstrand
    • 3
  1. 1.Department of BiologyCalifornia State UniversityChicoUSA
  2. 2.USDA/ARS, Exotic and Invasive Weeds UnitUniversity of Nevada, RenoRenoUSA
  3. 3.Department of Botany and Plant Sciences and Center for Conservation BiologyUniversity of CaliforniaRiversideUSA

Personalised recommendations