Biological Invasions

, Volume 11, Issue 5, pp 1107–1119 | Cite as

The role of intraspecific hybridization in the evolution of invasiveness: a case study of the ornamental pear tree Pyrus calleryana

Original Paper

Abstract

Hybridization between genetically distinct populations of a single species can serve as an important stimulus for the evolution of invasiveness. Such intraspecific hybridization was examined in Pyrus calleryana, a Chinese tree species commonly planted as an ornamental in residential and commercial areas throughout the United States. This self-incompatible species is now escaping cultivation and appearing in disturbed habitats, where it has the potential to form dense thickets. Using genetic techniques incorporating nine microsatellite markers, we show that abundant fruit set on cultivated trees as well as the subsequent appearance of wild individuals result from crossing between genetically distinct horticultural cultivars of the same species that originated from different areas of China. We conclude that intraspecific hybridization can be a potent but little recognized process impacting the evolution of invasiveness in certain species.

Keywords

Callery Pear Evolution Intraspecific hybridization Pyrus calleryana Self-incompatibility 

References

  1. Abbott RJ (1992) Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol Evol 7:401–405CrossRefGoogle Scholar
  2. Aïnouche ML, Baumel A, Salmon A, Yannic G (2003) Hybridization, polyploidy and speciation in Spartina (Poaceae). New Phytol 161:165–172CrossRefGoogle Scholar
  3. Anderson NO, Ascher PD (1993) Male and female fertility of loosestrife (Lythrum) cultivars. J Am Soc Hortic Sci 118:851–858Google Scholar
  4. Anderson E, Stebbins GL (1954) Hybridization as an evolutionary stimulus. Evolution 8:378–388CrossRefGoogle Scholar
  5. Anderson NO, Galatowitsch SM, Gomez N (2006) Selection strategies to reduce invasive potential in introduced plants. Euphytica 148:203–216CrossRefGoogle Scholar
  6. Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New YorkGoogle Scholar
  7. Baker H (1974) The evolution of weeds. Annu Rev Ecol Syst 5:1–24CrossRefGoogle Scholar
  8. Bando J (2005) Rapid evolution and the spread of introduced species: new insights from Spartina alterniflora invasions. Meeting of the Ecological Society of America, MontrealGoogle Scholar
  9. Burt JW, Muir AA, Piovia-Scott J, Veblan KE, Chang AL, Grossman JD, Weiskel HW (2007) Preventing horticultural introductions of invasive plants: potential efficacy of voluntary initiatives. Biol Invasions . doi:10.1007/s10530-007-9090-4 Google Scholar
  10. Clarke MM, Reichard SH, Hamilton CW (2006) Prevalence of different horticultural taxa of ivy (Hedera spp., Araliaceae) in invading populations. Biol Invasions 8:149–157CrossRefGoogle Scholar
  11. Cox GW (2004) Alien species and evolution: the evolutionary ecology of exotic plants, animals, microbes, and interacting native systems. Island Press, WashingtonGoogle Scholar
  12. Cuizhi G, Spongberg SA (2003) Pyrus. Flora of China 9:173–179Google Scholar
  13. Culley TM, Hardiman NA (2007) The beginning of a new invasive species: history and spread of the ornamental Callery Pear tree in the United States. Bioscience 57:956–964CrossRefGoogle Scholar
  14. Cunningham IS (1984) Frank N. Meyer: plant hunter in Asia. The Iowa State University Press, AmesGoogle Scholar
  15. Darlington CD (1940) Taxonomic species and genetic systems. In: Huxley J (ed) The new systematics. Clarendon Press, OxfordGoogle Scholar
  16. 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
  17. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050PubMedCrossRefGoogle Scholar
  18. Erickson DL, Fenster CB (2006) Intraspecific hybridization and the recovery of fitness in the native legume Chamaecrista fasciculata. Evolution 60:225–233PubMedGoogle Scholar
  19. Facon B, Jarne P, Pointier JP, David P (2005) Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigor is more important than increase in genetic variance. J Evol Biol 18:524–535PubMedCrossRefGoogle Scholar
  20. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  21. Farkas A, Orosz-Kovacs Z, Szabo LG (2002) Insect attraction of flowers in pear cultivars. In: Janick J, Sansavini S, Tagliavini M, Sugar D, Webster AD (eds) Proceedings of the VIIIth international symposium on Pear. Acta Horticulturae n. 596, ISHS pp 773–776Google Scholar
  22. Genton BJ, Dhykoff JA, Giraud T (2005) High genetic diversity in French invasive populations of common ragweed, Ambrosia artemisiifolia, as a result of multiple sources of introduction. Mol Ecol 14:4275–4285PubMedGoogle Scholar
  23. Gianfranceschi L, Seglias N, Tarchini R, Komjane M, Gessler C (1998) Simple sequence repeats for the genetic analysis of apple. Theor Appl Genet 96:1069–1076CrossRefGoogle Scholar
  24. Gilman EF, Watson DG (1994) Pyrus calleryana ‘Bradford’: ‘Bradford’ Callery pear. Fact Sheet ST-537, Environmental Horticulture Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of FloridaGoogle Scholar
  25. Hardiman NA, Culley TM (2007) Genetic analysis of Callery Pear cultivars to determine the origin of invasive populations. In: Cavender N (ed) Ohio invasive plant research conference proceedings, Ohio Biological Survey, Columbus, pp 59–66Google Scholar
  26. Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155CrossRefGoogle Scholar
  27. Husband BC, Barrett SCH (1991) Colonization history and population genetic structure of Eichhornia paniculata in Jamaica. Heredity 66:287–296CrossRefGoogle Scholar
  28. Jackson JE (2003) Biology of apples and pears. Cambridge University Press, CambridgeGoogle Scholar
  29. Johansen-Morris AD, Latta RG (2006) Fitness consequences of hybridization between ecotypes of Avena barbata: Hybrid breakdown, hybrid vigor, and transgressive segregation. Evolution 60:1585–1595PubMedGoogle Scholar
  30. Johnston AJ, Dieters MJ, Dungey HS, Nikles DG (2003) Intraspecific hybridization in Pinus caribaea var. hondurensis II. Genetic parameters. Euphytica 129:159–168CrossRefGoogle Scholar
  31. Khanduri VP, Sharma CM (2002) Intraspecific hybridization in Pinus roxburghii Sargent. Curr Sci 82:1003–1005Google Scholar
  32. Kitajima K, Fox A, Sato T, Nagamatsu D (2006) Cultivar selection prior to introduction may increase invasiveness: evidence from Ardisia crenata. Biol Invasions 8:1471–1482CrossRefGoogle Scholar
  33. Kolbe JJ, Gor RE, Rodriguez Schettino L, Chamizo Lara A, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181PubMedCrossRefGoogle Scholar
  34. Lavergne S, Molofsky J (2004) Reed canary grass (Phalaris arundinaceae) as a biological model in the study of plant invasions. Crit Rev Plant Sci 23:415–429CrossRefGoogle Scholar
  35. 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
  36. Lavoie C, Dufresne C (2005) The spread of reed canarygrass (Phalaris arundinacea) in Quebec: a spatio-temporal perspective. Ecoscience 12:366–375CrossRefGoogle Scholar
  37. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  38. Lee PLM, Patel RM, Conlan RS, Wainwright SJ, Hipkin CR (2004) Comparison of genetic diversities in native and alien populations of hoary mustard (Hirschfeldia incana [L.] Lagreze-Fossat). Int J Plant Sci 165:833–843CrossRefGoogle Scholar
  39. Lehrer JM, Brand MH, Lubell JD (2006) Four cultivars of Japanese Barberry demonstrate differential reproductive potential under landscape conditions. HortScience 41:762–767Google Scholar
  40. Lelong B, Lavoie C, Jodoin Y, Belzile F (2007) Expansion pathways of the exotic common reed (Phragmites australis): a historical and genetic analysis. Divers Distrib 13:430–437CrossRefGoogle Scholar
  41. Li Y, Cheng Z, Smith WA, Ellis DR, Chen Y, Zheng X, Pei Y, Luo K, Zhao D, Yao Q, Duan H, Li Q (2004) Invasive ornamental plants: problems, challenges, and molecular tools to neutralize their invasiveness. Crit Rev Plant Sci 23:381–389CrossRefGoogle Scholar
  42. Luken JO, Thieret JW (1996) Amur honeysuckle, its fall from grace. Bioscience 46:18–24CrossRefGoogle Scholar
  43. Merigliano MF, Lesica P (1998) The native status of reed canarygrass (Phalaris arundinacea L.) in the inland Northwest, USA. Nat Areas J 18:223–230Google Scholar
  44. Meyer FN (1918) Typescript of South China explorations. The special collections of the National Agricultural Library www.nal.usda.gov/speccoll/exhibits/meyer/meyer_typescript.html. Accessed 28 June 2007
  45. Novak SJ (2007) The role of evolution in the invasion process. Proc Natl Acad Sci USA 104:3671–3672PubMedCrossRefGoogle Scholar
  46. Novak SJ, Mack RN (1995) Allozyme diversity in the apomictic vine Bryonia alba (Cucurbitaceae): potential consequences of multiple introductions. Am J Bot 82:1153–1162CrossRefGoogle Scholar
  47. Novak SJ, Mack RN (2005) Genetic bottlenecks in alien plant species: influence of mating systems and introduction dynamics. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates, Inc. Publishers, Sunderland, pp 201–228Google Scholar
  48. Orson RA (1999) A paleoecological assessment of Phragmites australis in New England tidal marshes: changes in plant community structure during the last few millennia. Biol Invasions 1:149–158CrossRefGoogle Scholar
  49. Phillips L (2004) The 2005 urban tree of the year. City Trees 40:34–38Google Scholar
  50. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  51. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  52. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539PubMedCrossRefGoogle Scholar
  53. Poulin J, Weller SG, Sakai AK (2005) Genetic diversity does not affect the invasiveness of fountain grass (Pennisetum setaceum) in Arizona, California and Hawaii. Divers Distrib 11:241–247CrossRefGoogle Scholar
  54. Price SC, Jain SK (1981) Are inbreeders better colonizers? Oecologia 49:283–286CrossRefGoogle Scholar
  55. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201PubMedCrossRefGoogle Scholar
  56. Reichard SH, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51:103–113CrossRefGoogle Scholar
  57. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464PubMedCrossRefGoogle Scholar
  58. Roy J (1990) In search of the characteristics of plant invaders. In: di Castri F, Hansen AJ, Debussche M (eds) Biological invasions in Europe and the Mediterranean Basin. Kluwer Academic Publishers, Dordrecht, pp 335–352Google Scholar
  59. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  60. Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:2445–2449PubMedCrossRefGoogle Scholar
  61. Schierenbeck KA (2004) Japanese honeysuckle (Lonicera japonica) as an invasive species; history, ecology, and context. Crit Rev Plant Sci 23:391–400CrossRefGoogle Scholar
  62. Schierenbeck KA, Aïnouche ML (2006) The role of evolutionary genetics in studies of plant invasions. In: Cadotte MW, McMahon SM, Fukami T (eds) Conceptual ecology and invasion biology: reciprocal approaches to nature. Springer, Dordrecht, pp 193–221CrossRefGoogle Scholar
  63. Schiffman PM (1997) Animal-mediated dispersal and disturbance: driving forces behind alien plant naturalization. In: Luken JO, Thieret JW (eds) Assessment and management of plant invasions. Springer-Verlag, New York, pp 87–94Google Scholar
  64. Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573PubMedCrossRefGoogle Scholar
  65. Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New YorkGoogle Scholar
  66. Stebbins GL (1959) The role of hybridization in evolution. Proc Am Philos Soc 103:231–251Google Scholar
  67. Stebbins GL (1969) The significance of hybridization for plant taxonomy and evolution. Taxon 18:26–35CrossRefGoogle Scholar
  68. Swearingen J, Reshetiloff K, Slattery B, Zwicker S (2002) Plant invaders of mid-Atlantic natural areas. National Park Service and US Fish and Wildlife Service, WashingtonGoogle Scholar
  69. Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8:895–908CrossRefGoogle Scholar
  70. Taylor CM, David HG, Cicille JC, Grevstad FS, Hastings A (2004) Consequences of an Allee effect in the invasion of a Pacific estuary by Spartina alterniflora. Ecology 85:3254–3266CrossRefGoogle Scholar
  71. Vincent MA (2005) On the spread and current distribution of Pyrus calleryana in the United States. Castanea 70:20–31CrossRefGoogle Scholar
  72. Whitehouse WE, Creech JL, Seaton GA (1963) Bradford ornamental pear—a promising shade tree. Am Nurseryman 117(7–8):56–60Google Scholar
  73. Wilcox KL, Petrie SA, Maynard LA, Meyer SW (2003) Historical distribution and abundance of Phragmites australis at Long Point, Lake Erie, Ontario. J Great Lakes Res 29:664–680CrossRefGoogle Scholar
  74. 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
  75. Williams DA, Muchugu E, Overholt WA, Cuda JP (2007) Colonization patterns of the invasive Brazilian peppertree, Schinus terebinthifolius, in Florida. Heredity 98:284–293PubMedCrossRefGoogle Scholar
  76. Wilson SB, Knox GW (2006) Landscape performance, flowering, and seed viability of 15 Japanese Silver Grass cultivars grown in Northern and Southern Florida. Horttechnology 16:686–693Google Scholar
  77. Wolfe LM, Blair AC, Penna BM (2007) Does intraspecific hybridization contribute to the evolution of invasiveness? An experimental test. Biol Invasions 9:515–521CrossRefGoogle Scholar
  78. Yamamoto T, Kimura T, Sawamura Y, Manabe T, Kotobuki K, Hayashi T, Ban Y, Matsuta N (2002) Simple sequence repeats for genetic analysis in pear. Euphytica 124:129–137CrossRefGoogle Scholar
  79. Zielinski QB (1965) Self-incompatibility in Pyrus species. Bull Torrey Bot Club 92:219–220CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of CincinnatiCincinnatiUSA

Personalised recommendations