Skip to main content

Genetic characterization of hybridization between native and invasive bittersweet vines (Celastrus spp.)

Abstract

Hybridization associated with species introductions can accelerate the decline of native species. The main objective of this study was to determine if the decline of a North American liana (American bittersweet, Celastrus scandens) in the eastern portion of its range is related to hybridization with an introduced congener (oriental bittersweet, C. orbiculatus). We used newly characterized microsatellite loci, a maternally-inherited chloroplast DNA marker, and field observation to survey individuals across the USA to determine the prevalence of hybrids, their importance in the invasion of C. orbiculatus, and the predominant direction of hybridization. We found that only 8.4 % of non-native genotypes were hybrids (20 of 239), and these hybrids were geographically widespread. Hybrids showed reduced seed set (decline of >98 %) and small, likely inviable pollen. Genetic analysis of a maternally inherited chloroplast marker showed that all 20 identified hybrids came from C. scandens seed parents. The strong asymmetry in pollen flow that favors fecundity in introduced males has the potential to greatly accelerate the decline of native species by wasting limited female reproductive effort.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Adamack AT, Gruber B (2014) PopGenReport: simplifying basic population genetic analyses in R. Methods Ecol Evol 5:384–387. doi:10.1111/2041-210x.12158

    Article  Google Scholar 

  • Agresti A, Coull BA (1998) Approximate is better than “exact” for interval estimation of binomial proportions. Am Stat 52:119–126. doi:10.2307/2685469

    Google Scholar 

  • Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622

    Article  Google Scholar 

  • Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229

    PubMed Central  CAS  PubMed  Google Scholar 

  • Anttila CK, Daehler CC, Rank NE, Strong DR (1998) Greater male fitness of a rare invader (Spartina alterniflora, Poaceae) threatens a common native (Spartina foliosa) with hybridization. Am J Bot 85:1597–1601

    CAS  Article  PubMed  Google Scholar 

  • Ashton IW, Lerdau MT (2008) Tolerance to herbivory, and not resistance, may explain differential success of invasive, naturalized, and native North American temperate vines. Divers Distrib 14:169–178. doi:10.1111/j.1472-4642.2007.00425.x

    Article  Google Scholar 

  • Ayres DR, Zaremba K, Sloop CM, Strong DR (2008) Sexual reproduction of cordgrass hybrids (Spartina foliosa × alterniflora) invading tidal marshes in San Francisco Bay. Divers Distrib 14:187–195. doi:10.1111/j.1472-4642.2007.00414.x

    Article  Google Scholar 

  • Barbour RC, Potts BM, Vaillancourt RE, Tibbits WN, Wiltshire RJE (2002) Gene flow between introduced and native Eucalyptus species. New Forest 23:177–191

    Article  Google Scholar 

  • Bleeker W, Schmitz U, Ristow M (2007) Interspecific hybridisation between alien and native plant species in Germany and its consequences for native biodiversity. Biol Conserv 137:248–253. doi:10.1016/j.biocon.2007.02.004

    Article  Google Scholar 

  • Bogler D (2011) Celastrus pollen. Missouri Pollen Project. http://www.davidbogler.com/Pollen/key/Celastrus.html. Accessed 13 Sep 2011

  • Boyer MC, Muhlfeld CC, Allendorf FW (2008) Rainbow trout (Oncorhynchus mykiss) invasion and the spread of hybridization with native westslope cutthroat trout (Oncorhynchus clarkii lewisi). Can J Fish Aquat Sci 65:658–669. doi:10.1139/f08-001

    Article  Google Scholar 

  • Brizicky GC (1964) The genera of Celastrales in the southeastern United States. J Arnold Arboretum 45:206–234

    Google Scholar 

  • Buggs RJA, Pannell JR (2006) Rapid displacement of a monoecious plant lineage is due to pollen swamping by a dioecious relative. Curr Biol 16:996–1000. doi:10.1016/j.cub.2006.03.093

    CAS  Article  PubMed  Google Scholar 

  • Burgess KS, Husband BC (2006) Habitat differentiation and the ecological costs of hybridization: the effects of introduced mulberry (Morus alba) on a native congener (M. rubra). J Ecol 94:1061–1069. doi:10.1111/j.1365-2745.2006.01152.x

    Article  Google Scholar 

  • Burgess KS, Morgan M, Deverno L, Husband BC (2005) Asymmetrical introgression between two Morus species (M. alba, M. rubra) that differ in abundance. Mol Ecol 14:3471–3483

    CAS  Article  PubMed  Google Scholar 

  • Burgess KS, Morgan M, Husband BC (2008) Interspecific seed discounting and the fertility cost of hybridization in an endangered species. New Phytol 177:276–283. doi:10.1111/j.1469-8137.2007.02244.x

    PubMed  Google Scholar 

  • Davis CC, Webb CO, Wurdack KJ, Jaramillo CA, Donoghue MJ (2005) Explosive radiation of Malpighiales supports a mid-Cretaceous origin of modern tropical rain forests. Am Nat 165:E36–E65. doi:10.1086/428296

    Article  PubMed  Google Scholar 

  • Del Tredici P (2014) Untangling the twisted tale of oriental bittersweet. Arnoldia 71:2–18

    Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    Google Scholar 

  • Dreyer GD, Baird LM, Fickler C (1987) Celastrus scandens and Celastrus orbiculatus: comparisons of reproductive potential between a native and introduced woody vine. Bull Torrey Bot Club 114:260–264

    Article  Google Scholar 

  • 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 15:122–133

    CAS  Article  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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x

    CAS  Article  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. doi:10.1111/j.1471-8286.2007.01758.x

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Fike J, Niering WA (1999) Four decades of old field vegetation development and the role of Celastrus orbiculatus in the northeastern United States. J Veg Sci 10:483–492

    Article  Google Scholar 

  • Galpern P, Manseau M, Hettinga P, Smith K, Wilson P (2012) Allelematch: an R package for identifying unique multilocus genotypes where genotyping error and missing data may be present. Mol Ecol Resour 12:771–778. doi:10.1111/j.1755-0998.2012.03137.x

    Article  PubMed  Google Scholar 

  • Glenn TC, Schable NA (2005) Isolating microsatellite DNA loci. Mol Evol Prod Biochem Data Part B 395:202–222

    CAS  Article  Google Scholar 

  • Hall RJ, Hastings A, Ayres DR (2006) Explaining the explosion: modelling hybrid invasions. Proc R Soc B Biol Sci 273:1385–1389. doi:10.1098/rspb.2006.3473

    Article  Google Scholar 

  • Hegarty MJ, Barker GL, Brennan AC, Edwards KJ, Abbott RJ, Hiscock SJ (2009) Extreme changes to gene expression associated with homoploid hybrid speciation. Mol Ecol 18:877–889. doi:10.1111/j.1365-294X.2008.04054.x

    CAS  Article  PubMed  Google Scholar 

  • Hoban SM, McCleary TS, Schlarbaum SE, Romero-Severson J (2009) Geographically extensive hybridization between the forest trees American butternut and Japanese walnut. Biol Lett 5:324–327. doi:10.1098/rsbl.2009.0031

    PubMed Central  Article  PubMed  Google Scholar 

  • Hou D (1955) A revision of the genus Celastrus. Ann Mo Bot Gard 42:215–302

    Article  Google Scholar 

  • Hovick SM, Whitney KD (2014) Hybridisation is associated with increased fecundity and size in invasive taxa: meta-analytic support for the hybridisation-invasion hypothesis. Ecol Lett 17:1464–1477

    PubMed Central  Article  PubMed  Google Scholar 

  • Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biol Conserv 89:143–152

    Article  Google Scholar 

  • Jordano P, Godoy JA (2000) RAPD variation and population genetic structure in Prunus mahaleb (Rosaceae), an animal-dispersed tree. Mol Ecol 9:1293–1305. doi:10.1046/j.1365-294x.2000.01009.x

    CAS  Article  PubMed  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026. doi:10.1111/j.1365-294X.2008.03887.x

    Article  PubMed  Google Scholar 

  • Kibbe WA (2007) OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 35:W43–W46. doi:10.1093/nar/gkm234

    PubMed Central  Article  PubMed  Google Scholar 

  • Kishi S, Nishida T, Tsubaki Y (2009) Reproductive interference determines persistence and exclusion in species interactions. J Anim Ecol 78:1043–1049. doi:10.1111/j.1365-2656.2009.01560.x

    Article  PubMed  Google Scholar 

  • Kolbe JJ, Glor RE, Schettino LRG, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181. doi:10.1038/nature02807

    CAS  Article  PubMed  Google Scholar 

  • Kosman E, Leonard KJ (2005) Similarity coefficients for molecular markers in studies of genetic relationships between individuals for haploid, diploid, and polyploid species. Mol Ecol 14:415–424. doi:10.1111/j.1365-294X.2005.02416.x

    CAS  Article  PubMed  Google Scholar 

  • Lambertini C, Mendelssohn IA, Gustafsson MHG, Olesen B, Riis T, Sorrell BK, Brix H (2012) Tracing the origin of Gulf Coast Phragmites (Poaceae): a story of long-distance dispersal and hybridization. Am J Bot 99:538–551

    CAS  Article  PubMed  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. doi:10.1073/pnas.0607324104

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Leicht SA (2005) The comparative ecology of an invasive bittersweet species (Celastrus orbiculatus) and its native congener (C. scandens). Dissertation, University of Connecticut

  • Leicht-Young SA, Pavlovic NB, Grundel R, Frohnapple KJ (2007a) Distinguishing native (Celastrus scandens L.) and invasive (C. orbiculatus Thunb.) bittersweet species using morphological characteristics. J Torrey Bot Soc 134:441–450

    Article  Google Scholar 

  • Leicht-Young SA, Silander JA, Latimer AM (2007b) Comparative performance of invasive and native Celastrus species across environmental gradients. Oecologia 154:273–282. doi:10.1007/s00442-007-0839-3

    Article  PubMed  Google Scholar 

  • Leicht-Young SA, Latimer AM, Silander JA (2011) Lianas escape self-thinning: experimental evidence of positive density dependence in temperate lianas Celastrus orbiculatus and C. scandens. Perspect Plant Ecol Evol Syst 13:163–172

    Article  Google Scholar 

  • Levin DA, Francisco-Ortega J, Jansen RK (1996) Hybridization and the extinction of rare plant species. Conserv Biol 10:10–16

    Article  Google Scholar 

  • Mantel N (1967) Detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Maschinski J, Sirkin E, Fant J (2010) Using genetic and morphological analysis to distinguish endangered taxa from their hybrids with the cultivated exotic pest plant Lantana strigocamara (syn: Lantana camara). Conserv Genet 11:1607–1621. doi:10.1007/s10592-009-0035-6

    Article  Google Scholar 

  • Mercure M, Bruneau A (2008) Hybridization between the escaped Rosa rugosa (Rosaceae) and native R. blanda in eastern North America. Am J Bot 95:597–607. doi:10.3732/ajb.2007385

    CAS  Article  PubMed  Google Scholar 

  • Meyerson LA, Lambertini C, McCormick MK, Whigham DF (2012) Hybridization of common reed in North America? The answer is blowing in the wind. AoB Plants 2012:pls022 doi:10.1093/aobpla/pls022

  • Moody ML, Les DH (2007) Geographic distribution and genotypic composition of invasive hybrid watermilfoil (Myriophyllum spicatum x M. sibiricum) populations in North America. Biol Invasions 9:559–570. doi:10.1007/s10530-006-9058-9

    Article  Google Scholar 

  • Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420. doi:10.1093/bioinformatics/btp696

    CAS  Article  PubMed  Google Scholar 

  • Patterson DT (1974) The ecology of oriental bittersweet, Celastrus orbiculatus, a weedy introduced ornamental vine. Dissertation, Duke University

  • Pauls SU, Feldheim KA, Haase P (2007) Isolation and characterization of microsatellite markers in the caddisfly Drusus discolor (Trichoptera: Limnephilidae). Mol Ecol Notes 7:150–152. doi:10.1111/j.1471-8286.2006.01562.x

    CAS  Article  Google Scholar 

  • Pavlovic NB, Leicht-Young SA (2011) Are temperate mature forests buffered from invasive lianas? J Torrey Bot Soc 138:85–92

    Article  Google Scholar 

  • Pooler MR, Dix RL, Feely J (2002) Interspecific hybridizations between the native bittersweet, Celastrus scandens, and the introduced invasive species, C. orbiculatus. Southeast Nat 1:69–76

    Article  Google Scholar 

  • Prentis PJ, White EM, Radford IJ, Lowe AJ, Clarke AR (2007) Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis? New Phytol 176:902–912. doi:10.1111/j.1469-8137.2007.02217.x

    CAS  Article  PubMed  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing, 2.15.1 edn. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Rieseberg LH (2000) Crossing relationships among ancient and experimental sunflower hybrid lineages. Evolution 54:859–865. doi:10.1111/j.0014-3820.2000.tb00086.x

    CAS  Article  PubMed  Google Scholar 

  • Saltonstall K (2003) Microsatellite variation within and among North American lineages of Phragmites australis. Mol Ecol 12:1689–1702. doi:10.1046/j.1365-294X.2003.01849.x

    CAS  Article  PubMed  Google Scholar 

  • Saltonstall K, Castillo HE, Blossey B (2014) Confirmed field hybridization of native and introduced Phragmites australis (Poaceae) in North America. Am J Bot 101:211–215

    Article  PubMed  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    CAS  Article  PubMed  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573. doi:10.1038/sj.hdy.6885180

    Article  PubMed  Google Scholar 

  • Steward AM, Clemants SE, Moore G (2003) The concurrent decline of the native Celastrus scandens and spread of the non-native Celastrus orbiculatus in the New York City metropolitan area. Journal of the Torrey Botanical Society 130:143–146

    Article  Google Scholar 

  • Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74. doi:10.1093/nar/gkm306

    PubMed Central  Article  PubMed  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi:10.1111/j.1471-8286.2004.00684.x

    Article  Google Scholar 

  • Vilà M, D’Antonio CM (1998) Hybrid vigor for clonal growth in Carpobrotus (Aizoaceae) in coastal California. Ecol Appl 8:1196–1205

    Google Scholar 

  • White OE, Bowden WW (1947) Oriental and American bittersweet hybrids. J Hered 38:125–128

    CAS  PubMed  Google Scholar 

  • Winter DJ (2012) MMOD: an R library for the calculation of population differentiation statistics. Mol Ecol Resour 12:1158–1160. doi:10.1111/j.1755-0998.2012.03174.x

    CAS  Article  PubMed  Google Scholar 

  • Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053

    Article  Google Scholar 

  • Young JA, Young CG (1992) Seeds of woody plants in North America. Dioscorides Press, Portland, Oregon

    Google Scholar 

  • Zalapa JE, Brunet J, Guries RP (2009) Patterns of hybridization and introgression between invasive Ulmus pumila (Ulmaceae) and native U. rubra. Am J Bot 96:1116–1128. doi:10.3732/ajb.0800334

    CAS  Article  PubMed  Google Scholar 

  • Zaya DN (2013) Genetic characterization of invasion and hybridization: a bittersweet (Celastrus spp.) story. Department of Biological Sciences. Dissertation, University of Illinois at Chicago

Download references

Acknowledgments

We would like to thank Ralph Grundel and Krystal Frohnapple for assistance in planning and executing this study. Boris Igic, Jeremie Fant, Henry F. Howe, John Wilk, Emi Kuroiwa, Janet Backs, Eun Sun Kim, Jason Palagi, Wendy Stott, and Gina Morgan provided helpful comments that improved the manuscript. Sample collection was aided by Thomas Rawinksi, Ron Lance, John Balaban, Bob Stoos, and numerous National Park Service scientists. We would like to thank the National Park Service, Department of Environment and Conservation in Tennessee, DNR of Illinois, Indiana, and Michigan, North Carolina State Parks, and Forest Preserves Districts of Cook, Lake, and DuPage Counties in Illinois for permission to sample on their properties,. Microscopy and pollen grain measurement was aided by Jack Gibbons and Eun Sun Kim. Claudia Wing aided in development of the RFLP analysis. Genetic analysis was aided by Kirsten Dittel and Iryna Shak. Financial support was provided by the University of Illinois at Chicago, United States Geological Survey, and Chicago Wilderness. This article is contribution No. 1939 of the USGS Great Lakes Science Center. Use of trade, product, or firm names does not imply endorsement by the US Government. This manuscript was completed in partial fulfillment of the doctoral degree from the Graduate College at the University of Illinois at Chicago to D. N. Zaya.

Conflict of interest

The authors have no conflict of interest to report.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David N. Zaya.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 28 kb)

Supplementary material 2 (DOCX 53 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zaya, D.N., Leicht-Young, S.A., Pavlovic, N.B. et al. Genetic characterization of hybridization between native and invasive bittersweet vines (Celastrus spp.). Biol Invasions 17, 2975–2988 (2015). https://doi.org/10.1007/s10530-015-0926-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-0926-z

Keywords

  • Biological invasion
  • Celastrus
  • Hybridization
  • Microsatellite DNA
  • Population genetics