Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

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.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abbott RJ (1992) Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol Evol 7:401–405

    Article  Google Scholar 

  • Aïnouche ML, Baumel A, Salmon A, Yannic G (2003) Hybridization, polyploidy and speciation in Spartina (Poaceae). New Phytol 161:165–172

    Article  CAS  Google Scholar 

  • Anderson NO, Ascher PD (1993) Male and female fertility of loosestrife (Lythrum) cultivars. J Am Soc Hortic Sci 118:851–858

    Google Scholar 

  • Anderson E, Stebbins GL (1954) Hybridization as an evolutionary stimulus. Evolution 8:378–388

    Article  Google Scholar 

  • Anderson NO, Galatowitsch SM, Gomez N (2006) Selection strategies to reduce invasive potential in introduced plants. Euphytica 148:203–216

    Article  Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York

    Google Scholar 

  • Baker H (1974) The evolution of weeds. Annu Rev Ecol Syst 5:1–24

    Article  Google Scholar 

  • Bando J (2005) Rapid evolution and the spread of introduced species: new insights from Spartina alterniflora invasions. Meeting of the Ecological Society of America, Montreal

    Google Scholar 

  • 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 

  • Clarke MM, Reichard SH, Hamilton CW (2006) Prevalence of different horticultural taxa of ivy (Hedera spp., Araliaceae) in invading populations. Biol Invasions 8:149–157

    Article  Google Scholar 

  • Cox GW (2004) Alien species and evolution: the evolutionary ecology of exotic plants, animals, microbes, and interacting native systems. Island Press, Washington

    Google Scholar 

  • Cuizhi G, Spongberg SA (2003) Pyrus. Flora of China 9:173–179

  • 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 57:956–964

    Article  Google Scholar 

  • Cunningham IS (1984) Frank N. Meyer: plant hunter in Asia. The Iowa State University Press, Ames

    Google Scholar 

  • Darlington CD (1940) Taxonomic species and genetic systems. In: Huxley J (ed) The new systematics. Clarendon Press, Oxford

    Google Scholar 

  • 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 14:1697–1706

    Article  PubMed  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050

    Article  PubMed  CAS  Google Scholar 

  • Erickson DL, Fenster CB (2006) Intraspecific hybridization and the recovery of fitness in the native legume Chamaecrista fasciculata. Evolution 60:225–233

    PubMed  Google Scholar 

  • 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 18:524–535

    Article  PubMed  CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • 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 773–776

  • 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 14:4275–4285

    PubMed  CAS  Google Scholar 

  • Gianfranceschi L, Seglias N, Tarchini R, Komjane M, Gessler C (1998) Simple sequence repeats for the genetic analysis of apple. Theor Appl Genet 96:1069–1076

    Article  CAS  Google Scholar 

  • 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 Florida

  • 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 59–66

  • Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155

    Article  Google Scholar 

  • Husband BC, Barrett SCH (1991) Colonization history and population genetic structure of Eichhornia paniculata in Jamaica. Heredity 66:287–296

    Article  Google Scholar 

  • Jackson JE (2003) Biology of apples and pears. Cambridge University Press, Cambridge

    Google Scholar 

  • Johansen-Morris AD, Latta RG (2006) Fitness consequences of hybridization between ecotypes of Avena barbata: Hybrid breakdown, hybrid vigor, and transgressive segregation. Evolution 60:1585–1595

    PubMed  CAS  Google Scholar 

  • Johnston AJ, Dieters MJ, Dungey HS, Nikles DG (2003) Intraspecific hybridization in Pinus caribaea var. hondurensis II. Genetic parameters. Euphytica 129:159–168

    Article  CAS  Google Scholar 

  • Khanduri VP, Sharma CM (2002) Intraspecific hybridization in Pinus roxburghii Sargent. Curr Sci 82:1003–1005

    Google Scholar 

  • Kitajima K, Fox A, Sato T, Nagamatsu D (2006) Cultivar selection prior to introduction may increase invasiveness: evidence from Ardisia crenata. Biol Invasions 8:1471–1482

    Article  Google Scholar 

  • 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 431:177–181

    Article  PubMed  CAS  Google Scholar 

  • Lavergne S, Molofsky J (2004) Reed canary grass (Phalaris arundinaceae) as a biological model in the study of plant invasions. Crit Rev Plant Sci 23:415–429

    Article  Google Scholar 

  • Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888

    Article  PubMed  CAS  Google Scholar 

  • Lavoie C, Dufresne C (2005) The spread of reed canarygrass (Phalaris arundinacea) in Quebec: a spatio-temporal perspective. Ecoscience 12:366–375

    Article  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • 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 165:833–843

    Article  Google Scholar 

  • Lehrer JM, Brand MH, Lubell JD (2006) Four cultivars of Japanese Barberry demonstrate differential reproductive potential under landscape conditions. HortScience 41:762–767

    Google Scholar 

  • 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 13:430–437

    Article  Google Scholar 

  • 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 23:381–389

    Article  Google Scholar 

  • Luken JO, Thieret JW (1996) Amur honeysuckle, its fall from grace. Bioscience 46:18–24

    Article  Google Scholar 

  • Merigliano MF, Lesica P (1998) The native status of reed canarygrass (Phalaris arundinacea L.) in the inland Northwest, USA. Nat Areas J 18:223–230

    Google Scholar 

  • 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

  • Novak SJ (2007) The role of evolution in the invasion process. Proc Natl Acad Sci USA 104:3671–3672

    Article  PubMed  CAS  Google Scholar 

  • Novak SJ, Mack RN (1995) Allozyme diversity in the apomictic vine Bryonia alba (Cucurbitaceae): potential consequences of multiple introductions. Am J Bot 82:1153–1162

    Article  Google Scholar 

  • 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 201–228

    Google Scholar 

  • 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 1:149–158

    Article  Google Scholar 

  • Phillips L (2004) The 2005 urban tree of the year. City Trees 40:34–38

    Google Scholar 

  • Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • 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 52:273–288

    Article  Google Scholar 

  • 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 95:536–539

    Article  PubMed  CAS  Google Scholar 

  • 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 11:241–247

    Article  Google Scholar 

  • Price SC, Jain SK (1981) Are inbreeders better colonizers? Oecologia 49:283–286

    Article  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    Article  PubMed  CAS  Google Scholar 

  • Reichard SH, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51:103–113

    Article  Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    Article  PubMed  Google Scholar 

  • 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 335–352

    Google Scholar 

  • 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 32:305–332

    Article  Google Scholar 

  • Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:2445–2449

    Article  PubMed  CAS  Google Scholar 

  • Schierenbeck KA (2004) Japanese honeysuckle (Lonicera japonica) as an invasive species; history, ecology, and context. Crit Rev Plant Sci 23:391–400

    Article  Google Scholar 

  • 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 193–221

    Chapter  Google Scholar 

  • 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 87–94

    Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    Article  PubMed  Google Scholar 

  • Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York

    Google Scholar 

  • Stebbins GL (1959) The role of hybridization in evolution. Proc Am Philos Soc 103:231–251

    Google Scholar 

  • Stebbins GL (1969) The significance of hybridization for plant taxonomy and evolution. Taxon 18:26–35

    Article  Google Scholar 

  • 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, Washington

    Google Scholar 

  • Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8:895–908

    Article  Google Scholar 

  • 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 85:3254–3266

    Article  Google Scholar 

  • Vincent MA (2005) On the spread and current distribution of Pyrus calleryana in the United States. Castanea 70:20–31

    Article  Google Scholar 

  • Whitehouse WE, Creech JL, Seaton GA (1963) Bradford ornamental pear—a promising shade tree. Am Nurseryman 117(7–8):56–60

    Google Scholar 

  • 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 29:664–680

    Article  Google Scholar 

  • 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 14:3643–3656

    Article  PubMed  CAS  Google Scholar 

  • Williams DA, Muchugu E, Overholt WA, Cuda JP (2007) Colonization patterns of the invasive Brazilian peppertree, Schinus terebinthifolius, in Florida. Heredity 98:284–293

    Article  PubMed  CAS  Google Scholar 

  • Wilson SB, Knox GW (2006) Landscape performance, flowering, and seed viability of 15 Japanese Silver Grass cultivars grown in Northern and Southern Florida. Horttechnology 16:686–693

    Google Scholar 

  • Wolfe LM, Blair AC, Penna BM (2007) Does intraspecific hybridization contribute to the evolution of invasiveness? An experimental test. Biol Invasions 9:515–521

    Article  Google Scholar 

  • 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 124:129–137

    Article  CAS  Google Scholar 

  • Zielinski QB (1965) Self-incompatibility in Pyrus species. Bull Torrey Bot Club 92:219–220

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank D. Ayers, N. Ellstrand and K. Schierenbeck for organizing the symposium that led to this special issue, as well as enlightening discussions and comments on the manuscript. K. Manbeck provided an invaluable perspective from the green industry while M. Klooster, S. Rogstad and two anonymous reviewers provided helpful suggestions that greatly improved the manuscript. This research was supported by a grant from the US Department of Agriculture, Cooperative State Research, Education, and Extension Service, to T.M.C. (USDA CREES 06-35320-16565).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Cincinnati, 614 Rieveschl Hall, Cincinnati, OH, 45221-0006, USA

    Theresa M. Culley & Nicole A. Hardiman

Authors
  1. Theresa M. Culley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicole A. Hardiman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Theresa M. Culley.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Culley, T.M., Hardiman, N.A. The role of intraspecific hybridization in the evolution of invasiveness: a case study of the ornamental pear tree Pyrus calleryana . Biol Invasions 11, 1107–1119 (2009). https://doi.org/10.1007/s10530-008-9386-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-008-9386-z

Keywords

Search

Navigation