Conservation Genetics

, Volume 17, Issue 3, pp 593–602 | Cite as

Evidence for genetic erosion of a California native tree, Platanus racemosa, via recent, ongoing introgressive hybridization with an introduced ornamental species

  • Matthew G. Johnson
  • Kylene Lang
  • Paul Manos
  • Greg H. Golet
  • Kristina A. Schierenbeck
Research Article

Abstract

When non-native, genetically diverse species are introduced, hybridization with native congeners may erode the genetic composition of local species, perhaps even resulting in extinction. While such events may lead to adverse consequences at the community and ecosystem level, few studies exist on ecologically important tree species. In the genus Platanus, introgressive hybridization is widespread, and one common ornamental species, introduced to California during the late 19th century, is itself a hybrid. Our microsatellite analysis of more than 400 Platanus trees from north-central California reveals a complex pattern of invasion and hybridization in an age-structured population. By using size as a proxy for age, we have demonstrated that the Platanus population of north-central California has recently gained genetic diversity and effective population size. Principal coordinate analysis (PCoA) and genetic admixture analysis (STRUCTURE) both reveal a strong differentiation of genotypes into two main genetic clusters, with a large number of admixed genotypes. One of the genetic clusters identified is heavily biased towards younger trees, including samples from locations with relatively recently planted ornamental trees likely to be P. × hispanica (formerly known as P. × acerifolia). We conclude that the two genetic clusters correspond to the native P. racemosa and the introduced invasive hybrid species P. × hispanica. Additional hybridization between the invasive ornamental and the native species has occurred in California, and recent hybrid trees are more likely to be younger than trees without admixture. Our findings suggest that the observed increase in genetic diversity among California Platanus is due to rampant ongoing introgression, which may be threatening the continued genetic distinctiveness of the native species. This is cause for concern from a conservation standpoint, due to a direct loss of genetic distinctiveness, and a potential reduction in habitat value of associated species.

Keywords

Hybrid zone Admixture Sycamore Microsatellite 

Supplementary material

10592_2015_808_MOESM1_ESM.docx (119 kb)
Supplementary material 1 (DOCX 118 kb)

References

  1. Abbott RJ (1992) Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol Evol 7:401–405CrossRefPubMedGoogle Scholar
  2. Anselmi N, Cardin L, Nicolotti G (1994) Plane decline in European and Mediterranean countries: associated pests and their interactions. Bull OEPP/EPPO 24(1):159–171CrossRefGoogle Scholar
  3. 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 85:1597–1601CrossRefPubMedGoogle Scholar
  4. Avery TE, Burkhart HE (1983) Forest Measurements. McGraw-Hill Inc, New YorkGoogle Scholar
  5. Balao F, Casimiro-Soriguer R, García-Castraño JL, Terrab A, Talavera S (2015) Big thistle eats the little thistle: does unidirectional introgressive hybridization endanger the conservation of Onopordum hinojense? New Phytol 206:448–458CrossRefPubMedGoogle Scholar
  6. Baldwin B (2012) The Jepson manual: higher plants of California. University of California Press, BerkeleyGoogle Scholar
  7. Besnard G, Tagmount A, Baradat P, Vigouroux A, Berville A (2002) Molecular approach of genetic affinities between wild and ornamental Platanus. Euphytica 126:401–412CrossRefGoogle Scholar
  8. Buerkle CA (2005) Maximum-likelihood estimation of a hybrid index based on molecular markers. Mol Ecol Notes 5:684–687CrossRefGoogle Scholar
  9. 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 94:1061–1069CrossRefGoogle Scholar
  10. 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 14:3471–3483CrossRefPubMedGoogle Scholar
  11. Do C, Wapels RS, Peel D, Macbeth GM, Tillet BJ, Ovenden JR (2014) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Res 14:209–214CrossRefGoogle Scholar
  12. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242CrossRefGoogle Scholar
  13. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050CrossRefPubMedPubMedCentralGoogle Scholar
  14. Ernst WR (1963) The genera of Hamamelidaceae and Platanaceae in the southeastern United States. J Arnold Arbor 44:193–210Google Scholar
  15. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  16. Fant JB, Banai A, Havens K, Vitt P (2010) Hybridization between the threatened plant, Lespedeza leptostachya Englem. and its co-occurring congener Lespedeza capitata Michx.: morphological and molecular evidence. Conserv Genet. doi:10.1007/s10592-010-0105-9 Google Scholar
  17. Feng Y, Oh SH, Manos PS (2005) Phylogeny and historical biogeography of the genus Platanus as inferred from nuclear and chloroplast DNA. Syst Bot 30:786–799CrossRefGoogle Scholar
  18. Golet GH, Brown DL, Carlson M, Gardali T, Henderson A, Holl KD, Howell CA, Holyoak M, Hunt J, Kondolf GM, Larsen EW, Luster RA, McClain C, Nelson C, Paine S, Rainey W, Rubin Z, Shilling F, Silveira JG, Swagerty H, Williams NM, Wood D (2013) Successes, failures and suggested future directions for ecosystem restoration of the Middle Sacramento River, California. San Francisco Estuary and Watershed Science 11(3):1–29. http://www.escholarship.org/uc/item/0db0t6j1
  19. Griggs FT (2009) California riparian habitat restoration handbook, Second edition, River Partners, Chico. http://www.water.ca.gov/urbanstreams/docs/ca_riparian_handbook.pdf
  20. Grimm GW, Denk T (2008) ITS evolution in Platanus (Platanaceae): homeologues, pseudogenes and ancient hybridization. Ann Bot 101:403–419CrossRefPubMedPubMedCentralGoogle Scholar
  21. Henry A, Flood MG (1919) The history of the London plane (Platanus acerifolia). Notes on the genus Platanus. Proc Royal Ir Acad Sect B 35:9–28Google Scholar
  22. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefPubMedGoogle Scholar
  23. Lang K (2010) Microsatellite development in Platanus for documenting gene flow among species. Thesis. California State University, ChicoGoogle Scholar
  24. Mack MC, D’Antonio CM (1998) Impacts of biological invasions on disturbance regimes. Trends Ecol Evol 13:195–198CrossRefPubMedGoogle Scholar
  25. Meirmans P, Van Tienderen P (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  26. Muhlfeld CC, Kalinowski ST, McMahon TE, Taper ML, Painter S, Leary RF, Allendorf FW (2009) Hybridization rapidly reduces fitness of a native trout in the wild. Biol Lett 5:328–331CrossRefPubMedPubMedCentralGoogle Scholar
  27. Nixon KC, Poole JM (2003) Revision of the Mexican and Guatemalan species of Platanus (Platanaceae). Lundellia 6:103–137Google Scholar
  28. Oswald VH (2002) Selected plants of Northern California and adjacent Nevada. California State University, ChicoGoogle Scholar
  29. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research–an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  30. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  31. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109CrossRefGoogle Scholar
  32. Rieseberg LH, Wood TE, Baack A (2006) The nature of plant species. Nature 440:524–527CrossRefPubMedPubMedCentralGoogle Scholar
  33. Santamour FS Jr (1969) New chromosome counts in Ulmus and Platanus. Rhodora 71:544–547Google Scholar
  34. Santamour FS Jr (1972) Notes: interspecific hybridization in Platanus. For Sci 18(3):236–239Google Scholar
  35. Santamour FS, McArdle AJ (1986) Checklist of cultivated Platanus (Plane tree). J Arboric 12:78–83Google Scholar
  36. Smith DM, Finch DM (2014) Use of native and non-native nest plants by riparian-nesting birds along two streams in New Mexico. River Res Appl 30:1134–1145CrossRefGoogle Scholar
  37. Solek C, Szijj L (2004) Cactus wren (Campylorhynchus brunneicapillus). In: The Coastal Scrub and Chaparral Bird Conservation Plan: a strategy for protecting and managing coastal scrub and chaparral habitats and associated birds in California. California Partners in Flight. http://www.prbo.org/calpif/htmldocs/scrub.html
  38. Stralberg D, Toniolo V, Page GW, Stenzel LE (2004) Potential impacts of Spartina spread on shorebird populations in South San Francisco Bay. In: Proceedings of the third international conference on Invasive Spartina. 175–183Google Scholar
  39. Stuart JD, Sawyer JO (2001) Trees and shrubs of California. University of California Press, BerkeleyGoogle Scholar
  40. Sudworth GB (1967) Forest trees of the Pacific slope. Dover Publications Inc, New YorkGoogle Scholar
  41. USDA, NRCS (2008) The PLANTS Database. National Plant Data Center, Baton Rouge (http://plants.usda.gov. Accessed 24 Oct 2008)
  42. Vilà M, Weber E, Antonio CMD (2000) Conservation implications of invasion by plant hybridization. Biol Invasions 2:207–217CrossRefGoogle Scholar
  43. Waples RS, Do C (2008) LNDE: a program for estimating effective population size from allele frequency changes. Genetics 121:379–391Google Scholar
  44. Whitlock DL (2003) The hybridization of California sycamore (Platanus racemosa) and the London plane tree (Platanus × acerifolia) in California’s riparian woodland. Thesis. California State University, ChicoGoogle Scholar
  45. Zalapa JE, Brunet J, Guries RP (2009) Patterns of hybridization and introgression between invasive Ulmus pumila (Ulmaceae) and native U. rubra. Am J Bot 96:1116–1128CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Department of Plant SciencesChicago Botanic GardenGlencoeUSA
  2. 2.Department of Biological SciencesCalifornia State University-ChicoChicoUSA
  3. 3.Biology DepartmentDuke UniversityDurhamUSA
  4. 4.The Nature ConservancyChicoUSA

Personalised recommendations