Genetica

, Volume 129, Issue 2, pp 149–165 | Cite as

Hybridization and the colonization of novel habitats by annual sunflowers

  • Loren H. Rieseberg
  • Seung-Chul Kim
  • Rebecca A. Randell
  • Kenneth D. Whitney
  • Briana L. Gross
  • Christian Lexer
  • Keith Clay
Original Paper

Abstract

Although invasive plant species often have a hybrid ancestry, unambiguous evidence that hybridization has stimulated the evolution of invasive behaviors has been difficult to come by. Here, we briefly review how hybridization might contribute to the colonization of novel habitats, range expansions, and invasiveness and then describe work on hybrid sunflowers that forges a direct link between hybridization and ecological divergence. We first discuss the invasion of Texas by the common sunflower and show that the introgression of chromosomal segments from a locally adapted species may have facilitated range expansion. We then present evidence that the colonization of sand dune, desert floor, and salt marsh habitats by three hybrid sunflower species was made possible by selection on extreme or “transgressive” phenotypes generated by hybridization. This body of work corroborates earlier claims regarding the role of hybridization in adaptive evolution and provides an experimental and conceptual framework for ongoing studies in this area.

Keywords

Colonization Helianthus Hybridization Introgression Invasiveness QTLs Range expansion 

Notes

Acknowledgements

The research on sunflower hybridization described here has been supported by grants from the National Science Foundation, National Institutes of Health, and U.S. Department of Agriculture. This contribution was an invited paper for the 2004 Society for the Study of Evolution Symposium “All Stressed Out and Nowhere to Go: Does Evolvability Limit Adaptation in Invasive Species?”

References

  1. Abbott R (1992) Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol Evol 7:401–405CrossRefGoogle Scholar
  2. Abbott RJ, James JK, Milne RI, Gillies ACM (2003) Plant introductions, hybridization and gene flow. Phil Trans R Soc B 358:1123–1132PubMedCrossRefGoogle Scholar
  3. Ainouche ML, Baumel A, Salmon A, Yannic G (2003) Hybridization, polyploidy and speciation in Spartina (Poaceae). New Phytol 161:165–172CrossRefGoogle Scholar
  4. Al-Khatib K, Baumgartner JR, Peterson DE, Currie RS (1998) Imazethapyr resistance in common sunflower (Helianthus annuus). Weed Sci 46:403–407Google Scholar
  5. Anderson E (1948) Hybridization of the habitat. Evolution 2:1–9CrossRefGoogle Scholar
  6. Anderson E (1949) Introgressive hybridization. John Wiley and Sons, New YorkGoogle Scholar
  7. Anderson E, Stebbins GL (1954) Hybridization as an evolutionary stimulus. Evolution 8:378–388CrossRefGoogle Scholar
  8. Antonovics J (1976) The nature of limits to natural selection. Ann MO Bot Gard 63:224–247CrossRefGoogle Scholar
  9. Arnold ML (1997) Natural hybridization and evolution. Oxford Univ. Press, OxfordGoogle Scholar
  10. Arnold ML (2004) Transfer and origin of adaptations through natural hybridization: were Anderson and Stebbins right? Plant Cell 16:562–570PubMedCrossRefGoogle Scholar
  11. Arnold ML, Hodges SA (1995) Are natural hybrids fit or unfit relative to their parents? Trends Ecol Evol 10:67–71CrossRefGoogle Scholar
  12. Avise JC (1994) Molecular markers, natural history, and evolution. Chapman & Hall, New YorkGoogle Scholar
  13. Baker HG (1972) Migration of weeds. In: Valentine DH (ed) Taxonomy, phytogeography and evolution. Academic Press, London, pp 327–347Google Scholar
  14. Baker HG, Stebbins GL (1965) The genetics of colonizing species. Academic Press, New YorkGoogle Scholar
  15. Barrett SCH (1983) Crop mimicry in weeds. Econ Bot 37:255–282Google Scholar
  16. Barton NH (2001) The role of hybridisation in evolution. Mol Ecol 10:551–568PubMedCrossRefGoogle Scholar
  17. Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Ann Rev Ecol Syst 16:113–148CrossRefGoogle Scholar
  18. Blumler MA (2003) Introgression as a spatial phenomenon. Phys Geogr 24:414–432Google Scholar
  19. Buerkle CA, Morris RJ, Asmussen MA, Rieseberg LH (2000) The likelihood of homoploid hybrid speciation. Heredity 84:441–451PubMedCrossRefGoogle Scholar
  20. Buerkle CA, Wolf DE, Rieseberg LH (2003) The origin and extinction of species through hybridization. In: Brigham CA, Schwartz MW (eds) Population viability in plants. Springer Verlag, Berlin, pp 117–141Google Scholar
  21. Burke JM, Bulger MR, Wesselingh RA, Arnold ML (2000) Frequency and spatial patterning of clonal reproduction in Louisiana iris hybrid populations. Evolution 54:137–144PubMedCrossRefGoogle Scholar
  22. Burke JM, Lai Z, Salmaso M, Nakazato T, Tang S, Heesacker A, Knapp SJ, Rieseberg LH (2004) Comparative mapping and rapid karyotypic evolution in the genus Helianthus. Genetics 167:449–457PubMedCrossRefGoogle Scholar
  23. Chandler JM, Jan C, Beard BH (1986) Chromosomal differentiation among the annual Helianthus species. Syst Bot 11:353–371CrossRefGoogle Scholar
  24. Charlesworth D (1995) Evolution under the microscope. Curr Biol 5:835–836PubMedCrossRefGoogle Scholar
  25. Clausen J, Hiesey WM (1958) Experimental studies on the nature of species. IV. Genetic structure of ecological races. Carnegie Institute of Washington, Washington, DCGoogle Scholar
  26. deVicente MC, Tanksley SD (1993) QTL analysis of transgressive segregation in an interspecific tomato cross. Genetics 134:585–596PubMedGoogle Scholar
  27. Dorado O, Rieseberg LH, Arias D (1992) Chloroplast DNA introgression in southern California sunflowers. Evolution 46:566–572CrossRefGoogle Scholar
  28. Doebley J, Stec A, Gustus C (1995) Teosinte Branched1 and the origin of maize – evidence for epistasis and the evolution of dominance. Genetics 141:333–346PubMedGoogle Scholar
  29. Ellstrand NC (2003) Dangerous liaisons? When cultivated plants mate with their wild relatives. John Hopkins University Press, Balitmore, MDGoogle Scholar
  30. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci 97:7043–7050PubMedADSCrossRefGoogle Scholar
  31. Ellstrand NC, Whitkus R, Rieseberg LH (1996) Distribution of spontaneous plant hybrids. Proc Natl Acad Sci USA 93:5090–5093PubMedADSCrossRefGoogle Scholar
  32. Erlich PR (1989) Attributes of invaders and the invading process: vertebrates. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmanek M, Williamson M (eds) Biological invasions: a global perspective. John Wiley, London, pp 315–328Google Scholar
  33. Fritz RS, Moulia C, Newcombe G (1999) Resistance of hybrid plants and animals to herbivores, pathogens, and parasites. Annu Rev Ecol Syst 30:565–591CrossRefGoogle Scholar
  34. Fry JD (2003) Detecting ecological trade-offs using selection experiments. Ecology 84:1672–1678CrossRefGoogle Scholar
  35. Galatowitsch SM, Anderson NO, Ascher PD (1999) Invasiveness in wetland plants in temperate North America. Wetlands 19:733–755CrossRefGoogle Scholar
  36. Gaskin JF, Schaal BA (2002) Hybrid Tamarix widespread in US invasion and undetected in native Asian range. Proc Natl Acad Sci USA 99:11256–11259PubMedADSCrossRefGoogle Scholar
  37. Gottlieb LD (1972) Levels of confidence in the analysis of hybridization in plants. Ann MO Bot Gard 59:435–446CrossRefGoogle Scholar
  38. Grant V (1981) Plant speciation. Columbia Univ. Press, New YorkGoogle Scholar
  39. Grant PR, Grant BR (1992) Hybridization of bird species. Science 256:193–197ADSCrossRefPubMedGoogle Scholar
  40. Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711PubMedADSCrossRefGoogle Scholar
  41. Gray AJ, Marshall DF, Raybould AF (1991) A century of evolution in Spartina anglica. Adv Ecol Res 21:1–62MATHCrossRefGoogle Scholar
  42. Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194CrossRefGoogle Scholar
  43. Gross BL, Rieseberg LH (2005) The ecological genetics of homoploid hybrid speciation. J Hered 96:241–252PubMedCrossRefGoogle Scholar
  44. Gross BL, Schwarzbach AE, Rieseberg LH (2003) Origin(s) of the diploid hybrid species Helianthus deserticola (Asteraceae). Am J Bot 90:1708–1719Google Scholar
  45. Gross BL, Kane NC, Lexer C, Ludwig F, Rosenthal DM, Donovan LA, Rieseberg LH (2004) Reconstructing the origin(s) of Helianthus deserticola: survivorship and selection on the desert floor. Am Nat 164:145–156PubMedCrossRefGoogle Scholar
  46. Grotkopp E, Rejmanek M, Rost TL (2002) Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 pine (Pinus) species. Am Nat 159:396–419CrossRefPubMedGoogle Scholar
  47. Harlan JR, De Wet JMJ (1963) The compilospecies concept. Evolution 17:497–501CrossRefGoogle Scholar
  48. Harper JL (1977) Population biology of plants. Academic Press, New YorkGoogle Scholar
  49. Hauser L, Carvalho GR, Pitcher TJ, Ogutu-Ohwayo R (1998) Genetic affinities of an introduced predator: Nile perch in Lake Victoria, East Africa. Mol Ecol 7:849–857CrossRefGoogle Scholar
  50. Heiser CB (1947) Hybridization between the sunflower species Helianthus annuus and H. petiolaris. Evolution 1:249–262CrossRefGoogle Scholar
  51. Heiser CB (1949) Study in the evolution of the sunflower species Helianthus annuus and H. bolanderi. Univ Calif Publ Bot 23:157–196Google Scholar
  52. Heiser CB (1951a) Hybridization in the annual sunflowers: Helianthus annuus × H. argophyllus. Am Nat 85:64–72CrossRefGoogle Scholar
  53. Heiser CB (1951b) Hybridization in the annual sunflowers: Helianthus annuus × H. debilis var. cucumerifolius. Evolution 5:42–51CrossRefGoogle Scholar
  54. Heiser CB (1954) Variation and subspeciation in the common sunflower, Helianthus annuus. Am Midl Nat 51:287–305CrossRefGoogle Scholar
  55. Heiser CB (1965) Sunflowers, weeds, and cultivated plants. In: Barker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, Orlando, FL, pp 391–401Google Scholar
  56. Heiser CB, Smith DM, Clevenger S, Martin WC (1969) The North American sunflowers (Helianthus). Mem Torrey Bot Club 22:1–218Google Scholar
  57. Hoffmann AA, Blows MW (1994) Species borders: ecological and evolutionary perspectives. Trends Ecol Evol 9:223–227CrossRefGoogle Scholar
  58. Hubbs CL (1955) Hybridization between fish species in nature. Syst Zool 4:1–20CrossRefGoogle Scholar
  59. Johnston JA, Grise DJ, Donovan LA, Arnold ML (2001) Environment-dependent performance and fitness of Iris brevicaulis, I. fulva (Iridaceae), and hybrids. Am J Bot 88:933–938PubMedCrossRefGoogle Scholar
  60. Kim S-C, Rieseberg LH (1999) Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics 153:965–977PubMedGoogle Scholar
  61. Kim S-C, Rieseberg LH (2001) The contribution of epistasis to species differences in annual sunflowers. Mol Ecol 10:683–690PubMedCrossRefGoogle Scholar
  62. Kirkpatrick M, Barton NH (1997) Evolution of a species’ range. Am Nat 150:1–23CrossRefPubMedGoogle Scholar
  63. Lai Z, Nakazato T, Salmaso M, Burke JM, Tang S, Knapp SJ, Rieseberg LH (2005) Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics 171:1933:1940CrossRefGoogle Scholar
  64. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226CrossRefGoogle Scholar
  65. Langevin SA, Clay K, Grace JB (1990) The incidence and effects of hybridization between cultivated rice and its related weed red rice (Oryza sativa L.). Evolution 44:1000–1008CrossRefGoogle Scholar
  66. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  67. Levine JM, D’Antonio CM (1999) Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87:15–26CrossRefGoogle Scholar
  68. Lewontin RC, Birch LC (1966) Hybridization as a source of variation for adaptation to new environments. Evolution 20:315–336CrossRefGoogle Scholar
  69. Levin DA, Clay K (1984) Dynamics of synthetic Phlox drummondii populations at the species margin. Am J Bot 71:1040–1050CrossRefGoogle Scholar
  70. Lexer C, Welch M, Durphy JL, Rieseberg LH (2003a) Natural selection for salt tolerance QTL in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a homoploid hybrid species. Mol Ecol 12:1225–1235CrossRefGoogle Scholar
  71. Lexer C, Welch M, Raymond O, Rieseberg LH (2003b) The origins of ecological divergence in Helianthus paradoxus (Asteraceae): selection on transgressive characters in a novel hybrid habitat. Evolution 57:1989–2000CrossRefGoogle Scholar
  72. Lexer C, Rosenthal DM, Raymond O, Donovan L, Rieseberg LH (2005) Genetics of species differences in the wild annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 169:2225–2239PubMedCrossRefGoogle Scholar
  73. Lexer C, Lai Z, Rieseberg LH (2004) Candidate gene polymorphisms associated with salt tolerance in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. New Phytol 161:225–233CrossRefPubMedGoogle Scholar
  74. Ludwig F, Rosenthal D, Johnston JA, Kane N, Gross BL, Lexer C, Dudley SA, Rieseberg LH, Donovan LA (2004) Selection on leaf ecophysiological traits in a hybrid Helianthus species and early generation hybrids in a desert dune habitat. Evolution 58:2682–2692PubMedCrossRefGoogle Scholar
  75. Lynch M, Walsh B (1998) Genetics and the analysis of quantitative traits. Sinauer Associates, Sunderland, MAGoogle Scholar
  76. Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237PubMedCrossRefGoogle Scholar
  77. Marshall JK (1968) Factors limiting the survival of Corynephorus canescens (L.) Beauv. in Great Britain at the northern edge of its distribution. Oikos 19:206–216MathSciNetCrossRefGoogle Scholar
  78. Milne RI, Abbott RJ (2000) Origin and evolution of invasive naturalized material of Rhododendron ponticum L. in the British Isles. Mol Ecol 9:541–556PubMedCrossRefGoogle Scholar
  79. Moody ML, Les DH (2002) Evidence of hybridity in invasive watermilfoil (Myriophyllum) populations. Proc Natl Acad Sci USA 99:14867–14871PubMedADSCrossRefGoogle Scholar
  80. 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
  81. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304PubMedADSCrossRefGoogle Scholar
  82. Orians CM (2000) The effects of hybridization in plants on secondary chemistry: implications for the ecology and evolution of plant–herbivore interactions. Am J Bot 87:1749–1756PubMedCrossRefGoogle Scholar
  83. Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437PubMedCrossRefGoogle Scholar
  84. Pianka ER (1970) On r and K selection. Am Nat 102:592–597CrossRefGoogle Scholar
  85. Pimental D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. BioScience 50:53–65CrossRefGoogle Scholar
  86. Pires JC, Zhao JW, Schranz ME, Leon EJ, Quijada PA, Lukens LN, Osborn TC (2004) Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae). Biol J Linn Soc 82:675–688CrossRefGoogle Scholar
  87. Prince SD, Carter RN, Dancy KJ (1985) The geographical distribution of prickly lettuce (Lactuca serriola) II. Characteristics of populations near its distribution limit in Britain. J Ecol 73:39–48CrossRefGoogle Scholar
  88. Rattenbury JA (1962) Cyclic hybridization as a survival mechanism in the New Zealand forest flora. Evolution 16:348–363CrossRefGoogle Scholar
  89. Raven PH (1976) The bases of angiosperm phylogeny: cytology. Ann MO Bot Gard 62:409–451Google Scholar
  90. Rejmanek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1660CrossRefGoogle Scholar
  91. Rieseberg LH (1991) Homoploid reticulate evolution in Helianthus: evidence from ribosomal genes. Am J Bot 78:1218–1237CrossRefGoogle Scholar
  92. Rieseberg LH (2000) Crossing relationships among ancient and experimental sunflower hybrid lineages. Evolution 54:859–865PubMedCrossRefGoogle Scholar
  93. Rieseberg LH, Soltis DE (1991) Phylogenetic consequences of cytoplasmic gene flow in plants. Evol Trends Plants 5:65–84Google Scholar
  94. Rieseberg LH, Wendel J (1993) Introgression and its consequences in plants. In: Harrison R (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York, pp 70–114Google Scholar
  95. Rieseberg LH, Soltis DE, Palmer JD (1988) A molecular reexamination of introgression between Helianthus annuus and H. bolanderi. Evolution 42:227–238CrossRefGoogle Scholar
  96. Rieseberg LH, Beckstrom-Sternberg S, Doan K (1990a) Helianthus annuus ssp. texanus has chloroplast DNA and nuclear ribosomal RNA genes of Helianthus debilis ssp. cucumerifolius. Proc Natl Acad Sci USA 87:593–597ADSCrossRefGoogle Scholar
  97. Rieseberg LH, Carter R, Zona S (1990b) Molecular tests of the hypothesized hybrid origin of two diploid Helianthus species (Asteraceae). Evolution 44:1498–1511CrossRefGoogle Scholar
  98. Rieseberg LH, Beckstrom-Sternberg S, Liston A, Arias D (1991a) Phylogenetic and systematic inferences from chloroplast DNA and isozyme variation in Helianthus sect. Helianthus. Syst Bot 16:50–76CrossRefGoogle Scholar
  99. Rieseberg LH, Choi H, Ham D (1991b) Differential cytoplasmic versus nuclear gene flow in Helianthus. J Hered 82:489–493Google Scholar
  100. Rieseberg LH, Desrochers A, Youn SJ (1995a) Interspecific pollen competition as a reproductive barrier between sympatric species of Helianthus (Asteraceae). Am J Bot 82:515–519CrossRefGoogle Scholar
  101. Rieseberg LH, Van Fossen C, Desrochers A (1995b) Hybrid speciation accompanied by genomic reorganization in wild sunflowers. Nature 375:313–316ADSCrossRefGoogle Scholar
  102. Rieseberg LH, Sinervo B, Linder CR, Ungerer M, Arias DM (1996) Role of gene interactions in hybrid speciation: evidence from ancient and experimental hybrids. Science 272:741–745PubMedADSCrossRefGoogle Scholar
  103. Rieseberg LH, Archer MA, Wayne RK (1999a) Transgressive segregation, adaptation, and speciation. Heredity 83:363–372CrossRefGoogle Scholar
  104. Rieseberg LH, Whitton J, Gardner K (1999b) Hybrid zones and the genetic architecture of a barrier to gene flow between two wild sunflower species. Genetics 152:713–727Google Scholar
  105. Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, Durphy JL, Schwarzbach AE, Donovan LA, Lexer C (2003) Major ecological transitions in annual sunflowers facilitated by hybridization. Science 301:1211–1216PubMedADSCrossRefGoogle Scholar
  106. Rogers CE, Thompson TE, Seiler GJ (1982) Sunflower species of the United States. National Sunflower Association, Bismarck, NDGoogle Scholar
  107. Rosenthal DM, Rieseberg LH, Donovan LA (2005) Recreating ancient hybrid species’ complex multi-trait phenotypes from early generation synthetic hybrids: three examples using wild sunflowers. Am Nat 166:26–41PubMedCrossRefGoogle Scholar
  108. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughmann S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SC (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  109. Schemske DW (2000) Understanding the origin of species. Evolution 54:1069–1073CrossRefGoogle Scholar
  110. Schwarzbach AE, Rieseberg LH (2002) Likely multiple origins of a diploid hybrid sunflower species. Mol Ecol 11:1703–1717PubMedCrossRefGoogle Scholar
  111. Schwarzbach AE, Donovan LA, Rieseberg LH (2001) Transgressive character expression in a hybrid sunflower species. Am J Bot 88:270–277PubMedCrossRefGoogle Scholar
  112. Silander JA, Antonovics J (1979) The genetic basis of the ecological amplitude of Spartina patens. 1. Morphometric and physiological traits. Evolution 33:1114–1127CrossRefGoogle Scholar
  113. Small E (1984) Hybridization in the domesticated-weed-wild complex. In: Grant WF (ed) Plant biosystematics. Academic Press, Toronto, pp 195–210Google Scholar
  114. Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate JA, Mavrodiev E (2004) Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biol J Linn Soc 82:485–501CrossRefGoogle Scholar
  115. Sota T, Vogler AP (2001) Incongruence of mitochondrial and nuclear gene trees in Carabid beetles Ohomopterus. Syst Biol 50:39–59PubMedCrossRefGoogle Scholar
  116. Stace CA (1975) Hybridization and the Flora of the British Isles. Cambridge University Press, CambridgeGoogle Scholar
  117. Stebbins GL (1957) The hybrid origin of microspecies in the Elymus glaucus complex. Cytolo Suppl 36:336–340Google Scholar
  118. Stebbins GL (1959) The role of hybridization in evolution. Proc Am Phil Soc 103:231–251Google Scholar
  119. Stebbins GL (1969) The significance of hybridization for plant taxonomy and evolution. Taxon 18:26–35CrossRefGoogle Scholar
  120. Stebbins GL (1985) Polyploidy, hybridization, and the invasion of new habitats. Ann MO Bot Gard 72:824–832CrossRefGoogle Scholar
  121. Strauss SY (1994) Levels of herbivory and parasitism in host hybrid zones. Trends Ecol Evol 9:209–214CrossRefGoogle Scholar
  122. Sun M, Corke H (1992) Population genetics of colonizing success of weedy rye in Northern California. Theor Appl Genet 83:321–329CrossRefGoogle Scholar
  123. Tanksley SD (1993) Mapping polygenes. Annu Rev Genet 27:205–233PubMedCrossRefGoogle Scholar
  124. Thompson JD (1991) The biology of an invasive plant – what makes Spartina anglica so successful? Bioscience 41:393–401CrossRefGoogle Scholar
  125. Wang H, McArthur ED, Sanderson SC, Graham JH, Freeman DC (1997) Narrow hybrid zone between two subspecies of big sagebrush (Artemisia tridentata): Asteraceae. IV: reciprocal transplant experiments. Evolution 51:95–102CrossRefGoogle Scholar
  126. Wang RL, Wakeley J, Hey J (1997) Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics 147:1091–1106PubMedGoogle Scholar
  127. Weber E, D’Antonio CM (1999) Phenotypic plasticity in hybridizing Carpobrotus spp. (Aizoaceae) from coastal California and its role in plant invasion. Can J Bot/Rev Can Bot 77:1411–1418CrossRefGoogle Scholar
  128. Welch ME, Rieseberg LH (2002) Patterns of genetic variation suggest a single, ancient origin for the diploid hybrid species Helianthus paradoxus. Evolution 56:2126–2137PubMedCrossRefGoogle Scholar
  129. Wendel JF, Doyle JJ (1998) Phylogenetic incongruence: window into genome history and molecular evolution. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants II: DNA sequencing. Kluwer Academic Publishers, Boston, pp 256–296Google Scholar
  130. Wendel JF, Stewart JM, Rettig JH (1991) Molecular evidence for homoploid reticulate evolution among Australian species of Gossypium. Evolution 45:694–671CrossRefGoogle Scholar
  131. Wilkes HG (1977) Hybridization of maize and teosinte in Mexico and Guatemala and the improvement of maize. Econ Bot 31:254–293Google Scholar
  132. Williamson M (1996) Biological invasions. Chapman & Hall, LondonGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Loren H. Rieseberg
    • 1
  • Seung-Chul Kim
    • 2
  • Rebecca A. Randell
    • 1
  • Kenneth D. Whitney
    • 1
  • Briana L. Gross
    • 1
  • Christian Lexer
    • 3
  • Keith Clay
    • 1
  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA
  2. 2.Department of Botany and Plant ScienceUniversity of CaliforniaRiversideUSA
  3. 3.Jodrell LaboratoryRoyal Botanic Gardens KewRichmond, SurreyUK

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