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Ecological Genetics of Plant Invasion: What Do We Know?

Published online by Cambridge University Press:  20 January 2017

Sarah M. Ward*
Affiliation:
Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO 80523
John F. Gaskin
Affiliation:
USDA–ARS Northern Plains Agricultural Research Laboratory, Sidney, MT 59270
Linda M. Wilson
Affiliation:
Department of Plant, Soil, and Entomological Sciences, University of Idaho, Moscow, ID 83844
*
Corresponding author's E-mail: sarah.ward@colostate.edu

Abstract

The rate at which plant invasions occur is accelerating globally, and a growing amount of recent research uses genetic analysis of invasive plant populations to better understand the histories, processes, and effects of plant invasions. The goal of this review is to provide natural resource managers with an introduction to this research. We discuss examples selected from published studies that examine intraspecific genetic diversity and the role of hybridization in plant invasion. We also consider the conflicting evidence that has emerged from recent research for the evolution of increased competitiveness as an explanation for invasion, and the significance of multiple genetic characteristics and patterns of genetic diversity reported in the literature across different species invasions. High and low levels of genetic diversity have been found in different invading plant populations, suggesting that either selection leading to local adaptation, or pre-adapted characteristics such as phenotypic plasticity, can lead to aggressive range expansion by colonizing nonnative species. As molecular techniques for detecting hybrids advance, it is also becoming clear that hybridization is a significant component of some plant invasions, with consequences that include increased genetic diversity within an invasive species, generation of successful novel genotypes, and genetic swamping of native plant gene pools. Genetic analysis of invasive plant populations has many applications, including predicting population response to biological or chemical control measures based on diversity levels, identifying source populations, tracking introduction routes, and elucidating mechanisms of local spread and adaptation. This information can be invaluable in developing more effectively targeted strategies for managing existing plant invasions and preventing new ones. Future genetic research, including the use of high throughput molecular marker systems and genomic approaches such as microarray analysis, has the potential to contribute to better understanding and more effective management of plant invasions.

Type
Invited Review
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Abbott, R. J. 1992. Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol. Evol. 7:401405.CrossRefGoogle ScholarPubMed
Abbott, R. J., James, J. K., Milne, R. I., and Gillies, A. C. M. 2003. Plant introductions, hybridization and gene flow. Philos. T. Roy. Soc. B 358:11231132.CrossRefGoogle ScholarPubMed
Ainouche, M. L., Baumel, A., Salmon, A., and Yannic, G. 2004. Hybridization, polyploidy and speciation in Spartina (Poaceae). New Phytol. 161:65172.CrossRefGoogle Scholar
Amsellem, L., Noyer, J. L., Le Bourgeois, T., and Hossaert-McKey, M. 2000. Comparison of genetic diversity of the invasive weed Rubus alceifolius Poir. (Rosaceae) in its native range and in areas of introduction, using amplified fragment length polymorphism (AFLP) markers. Mol. Ecol. 9:443455.CrossRefGoogle ScholarPubMed
Anderson, E. C. 1949. Introgressive hybridization. New York Wiley. 109.CrossRefGoogle Scholar
Anttila, C. K., Daehler, C. C., Rank, N. E., and Strong, D. R. 1998. Greater male fitness of a rare invader (Spartina alterniflora, Poaceae) threatens a common native (Spartina foliosa) with hybridization. Am. J. Bot. 85:15971601.Google Scholar
Ayres, D. R. and Strong, D. R. 2001. Origin and genetic diversity of Spartina anglica (Poaceae) using nuclear DNA markers. Am. J. Bot. 88:18631867.CrossRefGoogle ScholarPubMed
Barbour, R. C., Potts, B. M., and Vaillancourt, R. E. 2006. Gene flow between introduced and native Eucalyptus species: early-age selection limits invasive capacity of exotic E. ovata × nitens F-1 hybrids. Forest Ecol. Manag. 228:206214.Google Scholar
Bleeker, W. 2003. Hybridization and Rorippa austriaca (Brassicaceae) invasion in Germany. Mol. Ecol. 12:18311841.Google Scholar
Blossey, B. and Notzold, R. 1995. What determines the increased competitive ability of invasive nonindigenous plants: a hypothesis. J. Ecol. 83:887889.CrossRefGoogle Scholar
Bossdorf, O., Auge, H., Lafuma, L., Rogers, W. E., Siemann, E., and Prati, D. 2005. Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:111.Google Scholar
Bossdorf, O., Prati, D., Aauge, H., and Schmid, B. 2004. Reduced competitive ability in an invasive plant. Ecol. Lett. 7:346353.CrossRefGoogle Scholar
Brock, M. T. 2004. The potential for genetic assimilation of a native dandelion species, Taraxacum ceratophorum (Asteraceae), by the exotic congener T. officinale . Am. J. Bot. 91:656663.CrossRefGoogle ScholarPubMed
Brown, B. J. and Mitchell, R. J. 2001. Competition for pollination: effects of pollen of an invasive plant on seed set of a native congener. Oecologia 129:4349.Google Scholar
Bruckart, W., Cavin, C., Vajna, L., Schwarczinger, I., and Ryan, F. J. 2004. Differential susceptibility of Russian thistle accessions to Colletotrichum gloeosporioides . Biol. Control 30:306311.Google Scholar
Burdon, J. J., Groves, R. H., and Cullen, J. M. 1981. The impact of biological control on the distribution and abundance of Chondrilla juncea in southeastern Australia. J. Appl. Ecol. 18:957966.CrossRefGoogle Scholar
Burdon, J. J., Groves, R. H., Kaye, P. E., and Speer, S. S. 1984. Competition in mixtures of susceptible and resistant genotypes of Chondrilla juncea differentially infected with rust. Oecologia 64:199203.CrossRefGoogle ScholarPubMed
Carter, M. C. and Sytsma, M. D. 2001. Comparison of the genetic structure of North and South American populations of a clonal aquatic plant. Biol. Invasions 3:113118.Google Scholar
Chapman, H. M., Parh, D., and Oraguzie, N. 2000. Genetic structure and colonizing success of a clonal, weedy species, Pilosella officinarum (Asteraceae). Heredity 84:401409.CrossRefGoogle ScholarPubMed
Crawley, M. 1987. What makes a community invasible? 229253. in Gray, A.J., Crawley, M.J., Edwards, P.J., eds. Colonization, Succession and Stability. London Blackwell Scientific. 482.Google Scholar
Daehler, C. C. 2003. Performance comparisons of co-occuring native and alien invasive plants: implications of conservation and restoration. Ann. Rev. Ecol. Evol. Syst. 34:183211.Google Scholar
D'Antonio, C. M. and Vitousek, P. M. 1992. Biological invasions by exotic grasses, the grass/fire cycle, and global change. Ann. Rev. Ecol. Evol. Syst. 23:6387.Google Scholar
DeWalt, S. J. and Hamrick, J. L. 2004. Genetic variation of introduced Hawaiian and native Costa Rican populations of an invasive tropical shrub, Clidemia hirta (Melastomataceae). Am. J. Bot. 91:11551162.CrossRefGoogle ScholarPubMed
Dong, M., Lu, B-R., Zhang, H-B., Chen, J-K., and Li, B. 2006. Role of sexual reproduction in the spread of an invasive clonal plant Solidago canadensis revealed using intersimple sequence repeat markers. Plant Species Biol. 21:1318.Google Scholar
Durka, W., Bossdorf, O., Prati, D., and Auge, H. 2005. Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol. Ecol. 14:16971706.Google Scholar
Ellstrand, N. C. and Elam, D. R. 1993. Population genetic consequences of small population size: implications for plant conservation. Ann. Rev. Ecol. Syst. 24:217242.Google Scholar
Ellstrand, N. C. and Schierenbeck, K. A. 2000. Hybridization as a stimulus for the evolution of invasiveness in plants? Proc. Natl. Acad. Sci. USA 97:70437050.Google Scholar
Ellstrand, N. C., Whitkus, R., and Rieseberg, L. H. 1996. Distribution of spontaneous plant hybrids. Proc. Natl. Acad. Sci. USA 93:50905093.Google Scholar
Fisher, R. A. 1930. The genetical theory of natural selection. Oxford Clarendon Press. 360.Google Scholar
Frankham, R. 2005. Resolving the genetic paradox in invasive species. Heredity 94:385.CrossRefGoogle ScholarPubMed
Gaskin, J. F. and Schaal, B. A. 2002. Hybrid Tamarix widespread in US invasion and undetected in native Asian range. Proc. Natl. Acad. Sci. USA 99:1125611259.Google Scholar
Geng, Y-P., Pan, X-Y., Xu, C-Y., Zhang, W-J., Li, B., Chen, J-K., Lu, B-R., and Song, Z-P. 2007. Phenotypic plasticity rather than locally adapted ecotypes allows the invasive alligator weed to colonize a wide range of habitats. Biol. Invasions 9:245256.Google Scholar
Genton, B. J., Shykoff, J. A., and 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. 14:42754285.Google Scholar
Goldberg, D. E. 1996. Competitive ability: definitions, contingency and correlated traits. Philos. Trans. Royal Soc. Lond. B 351:13771385.Google Scholar
Goolsby, J. A., De Barro, P. J., Makinson, J. R., Pemberton, R. W., Hartley, D. M., and Frohlich, D. R. 2006. Matching the origin of an invasive weed for selection of a herbivore haplotype for a biological control program. Mol. Ecol. 15:287297.Google Scholar
Hamrick, J. L. and Godt, M. J. 1983. The distribution of genetic variation within and among natural plant populations. Pages 335348. in Shonewald-Cox, C.M., Chambers, S.M., MacBryde, B., Thomas, L., eds. Genetics and Conservation. Menlo Park Cummings.Google Scholar
Hamrick, J. L. and Godt, M. J. 1996. Effects if life history traits on genetic diversity in plant species. Philos. Trans. Royal Soc. Lond. B. 351:12911298.Google Scholar
Hinz, H. L. and Schwarzlaender, M. 2004. Comparing invasive plants from their native and exotic range: what can we learn for biological control? Weed Technol. 18:15331541.Google Scholar
Hollingsworth, M. L. and Bailey, J. P. 2000. Evidence for massive clonal growth in the invasive weed Fallopia japonica (Japanese knotweed). Bot. J. Linn. Soc. 133:463472.CrossRefGoogle Scholar
Hopper, K. R., Roush, R. T., and Powell, W. 1993. Management of genetics of biological control introductions. Ann. Rev. Entomol. 38:2751.CrossRefGoogle Scholar
Jasieniuk, M. and Maxwell, B. D. 2001. Plant diversity: new insights from molecular biology and genomics technologies. Weed Sci. 49:257265.Google Scholar
Keane, R. M. and Crawley, M. J. 2002. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17:164170.Google Scholar
Lavergne, S. and Molofsky, J. 2007. Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc. Natl. Acad. Sci. USA 104:38833888.Google Scholar
Lee, C. E. 2002. Evolutionary genetics of invasive species. Trends Ecol. Evol. 17:386390.Google Scholar
Leger, E. A. and Rice, K. J. 2007. Assessing the speed and predictability of local adaptation in invasive California poppies (Eschscholzia californica). J. Evol. Biol. 20:10901103.Google Scholar
Levin, D. A., Francisco Ortega, J., and Jansen, R. K. 1996. Hybridization and the extinction of rare plant species. Conserv. Biol. 10:1016.Google Scholar
Lewontin, R. C. and Birch, L. C. 1966. Hybridization as a source of variation for adaptation to new environments. Evolution 20:315336.Google Scholar
Mack, R. N. 1991. The commercial seed trade: an early disperser of weeds in the United States. Econ. Bot. 45:257273.Google Scholar
Mack, R. N. and Lonsdale, W. M. 2001. Humans as global plant dispersers: getting more than we bargained for. BioScience 51/2:95102.CrossRefGoogle Scholar
Mack, R. N., Simberloff, D., Lonsdale, W. M., Evans, H., and Bazzaz, F. A. 2000. Biotic invasions: causes, epidemiology, global consequences and control. Ecol. Applic. 10:689710.Google Scholar
Mandak, B., Bimova, K., Pysek, P., Stepanek, J., and Plackova, I. 2005. Isoenzyme diversity in Reynoutria (Polygonaceae) taxa: escape from sterility by hybridization. Plant Syst. Evol. 253:219230.Google Scholar
Maron, J. L. and Vila, M. 2001. When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361373.CrossRefGoogle Scholar
Maron, J. L., Vila, M., Bommarco, R., Elmendorf, S., and Beardsley, P. 2004. Rapid evolution of an invasive plant. Ecol. Monographs 74/2:261280.CrossRefGoogle Scholar
Meimberg, H., Hammond, J. I., Jorgensen, C. M., Park, T. W., Gerlach, J. D., Rice, K. J., and McKay, J. K. 2006. Molecular evidence for an extreme genetic bottleneck during introduction of an invading grass to California. Biol. Invasions 8:13551366.Google Scholar
Mengistu, L. W. and Messersmith, C. G. 2002. Genetic diversity of kochia. Weed Sci. 50:498503.Google Scholar
Mengistu, L. W., Mueller-Warrant, G. W., and Barker, R. E. 2000. Genetic diversity of Poa annua in western Oregon grass seed. Theor. Appl. Genet. 101:7079.Google Scholar
Milne, R. I. and Abbott, R. J. 2000. Origin and evolution of invasive naturalized material of Rhododendron ponticum L. in the British Isles. Mol. Ecol. 9:541556.Google Scholar
Mohammadi, S. A. and Prasanna, B. M. 2003. Analysis of genetic diversity in crop plants—salient statistical tools and considerations. Crop Sci. 43:12351248.Google Scholar
Moody, M. L. and Les, D. H. 2002. Evidence of hybridity in invasive watermilfoil (Myriophyllum) populations. Proc. Natl. Acad. Sci. USA 99:1486714871.Google Scholar
Mooney, H. A. and Cleland, E. E. 2001. The evolutionary impact of invasive species. Proc. Natl. Acad. Sci. USA 98:54465451.Google Scholar
Nissen, S. J., Masters, R. A., Lee, D. J., and Rowe, M. L. 1995. DNA-based marker systems to determine genetic diversity of weedy species and their application to biocontrol. Weed Sci. 43:504513.Google Scholar
Novak, S. J. and Mack, R. N. 2001. Tracing plant introduction and spread: genetic evidence from Bromus tectorum (cheatgrass). BioScience 51/2:114122.Google Scholar
Parker, I. M., Rodriguez, J., and Loik, M. E. 2003. An evolutionary approach to understanding the biology of invasions: local adaptation and general-purpose genotypes in the weed Verbascum thapsus . Conserv. Biol. 17:5972.Google Scholar
Pester, T. A., Ward, S. M., Fenwick, A. L., Westra, P. J., and Nissen, S. J. 2003. Genetic diversity of jointed goatgrass (Aegilops cylindrica) determined with RADP and AFLP markers. Weed Sci. 51:287293.CrossRefGoogle Scholar
Petit, R. J. 2004. Biological invasions at the gene level. Divers. Distrib. 10:159165.Google Scholar
Poulin, J., Weller, S. G., and Sakai, A. K. 2005. Genetic diversity does not affect the invasiveness of fountain grass (Pennisetum setaceum) in Arizona, California and Hawaii. Divers. Distrib. 11:241247.Google Scholar
Pysek, P., Brock, J. H., Bimova, K., Mandak, B., Jarosik, V., Koukolikova, I., Pergl, J., and Stepanek, J. 2003. Vegetative regeneration in invasive Reynoutria (Polygonaceae) taxa: the determinant of invasibility at the genotype level. Am. J. Bot. 90:14871495.Google Scholar
Raybould, A. F., Gray, A. J., Lawrence, M. J., and Marshall, D. F. 1991. The evolution of Spartina anglica Hubbard (Gramineae) - origin and genetic variability. Biol. J. Linn. Soc. 43:111126.CrossRefGoogle Scholar
Ren, M. X., Zhang, Q. G., and Zhang, D. Y. 2005. Random amplified polymorphic DNA markers reveal low genetic variation and a single dominant genotype in Eichhornia crassipes populations throughout China. Weed Res. 45:236244.Google Scholar
Rhymer, J. M. and Simberloff, D. 1996. Extinction by hybridization and introgression. Ann. Rev. Ecol. Syst. 27:83109.Google Scholar
Rieseberg, L. H. 1997. Hybrid origins of plant species. Ann. Rev. Ecol. Syst. 28:59389.Google Scholar
Rieseberg, L. H., Kim, S. C., Randell, R. A., Whitney, K. D., Gross, B. L., Lexer, C., and Clay, K. 2007. Hybridization and the colonization of novel habitats by annual sunflowers. Genetica 129:149165.Google Scholar
Rowe, M. L., Lee, D. J., Nissen, S. J., Bowditch, B. M., and Masters, R. A. 1997. Genetic variation in North American leafy spurge (Euphorbia esula) determined by DNA markers. Weed Sci. 45:446454.Google Scholar
Sakai, A. K., Allendorf, F. W., Holt, J. S., Lodge, D. M., Molofsky, J., With, K. A., Baughman, S., Cabin, R. J., Cohen, J. E., Ellstrand, N. C., McCauley, D. E., O'Neill, P., Parker, I. M., Thompson, J. N., and Weller, S. G. 2001. The population biology of invasive species. Ann. Rev. Ecol. Syst. 32:305332.CrossRefGoogle 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 99:24452449.Google Scholar
Scheepens, J. F., Veeneklaas, R. M., Van de Zande, L., and Bakker, J. P. 2007. Clonal structure of Elytrigia atherica along different successional stages of a salt marsh. Mol. Ecol. 16:11151124.Google Scholar
Schlötterer, C. 2002. A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics 160:753763.Google Scholar
Siemann, E. and Rogers, W. E. 2001. Genetic differences in growth of an invasive tree species. Ecol. Lett. 4:514518.Google Scholar
Soltis, P. S. and Soltis, D. E. 2000. The role of genetic and genomic attributes in the success of polyploids. Proc. Natl. Acad. Sci. USA 97:70517057.Google Scholar
Stebbins, G. L. 1950. Variation and Evolution in Plants. New York Columbia University Press. 643.Google Scholar
Stebbins, G. L. 1959. The role of hybridization in evolution. Proc. Am. Philos. Soc. 103:231251.Google Scholar
Stebbins, G. L. 1969. The significance of hybridization for plant taxonomy and evolution. Taxon 18:2635.Google Scholar
Sultan, S. E. 1995. Phenotypic plasticity and plant adaptation. Acta Bot. Neerl. 44:363383.Google Scholar
Sun, J. H., Li, Z-C., Jewett, D. K., Britton, K. O., Ye, W. H., and Ge, X-J. 2005. Genetic diversity of Pueraria lobata (kudzu) and closely related taxa as revealed by inter-simple sequence repeat analysis. Weed Res. 45:255260.Google Scholar
Thebaud, C. and Simberloff, D. 2001. Are plants really larger in their introduced ranges? Am. Nat. 157:231236.Google Scholar
Van Kleunen, M. and Schmid, B. 2003. No evidence for an evolutionary increased competitive ability in an invasive plant. Ecology 84:28162823.Google Scholar
Via, S., Gomulkiewicz, R., De Jong, G., Scheiner, S. M., Schlichting, C. D., and Van Tienderen, P. H. 1995. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. Evol. 10:212217.Google Scholar
Vila, M. and D'Antonio, C. M. 1998. Hybrid vigor for clonal growth in Carpobrotus (Aizoaceae) in coastal California. Ecol. Appl. 8:11961205.Google Scholar
Vila, M., Gomez, A., and Maron, J. L. 2003. Are alien plants more competitive than their native conspecifics? A test using Hypericum perforatum L. Oecologia 137:211215.Google Scholar
Vila, M., Maron, J. L., and Marco, L. 2005. Evidence for the enemy release hypothesis in Hypericum perforatum . Oecologia 142:474479.CrossRefGoogle ScholarPubMed
Vila, M., Weber, E., and D'Antonio, C. M. 2000. Conservation implications of invasion by plant hybridization. Biol. Invasions 2:207217.Google Scholar
Vitousek, P. M., D'Antonio, C. M., Loope, L. I., and Westbrooks, R. 1996. Biological invasions as global environmental change. Am. Sci. 84:468478.Google Scholar
Ward, S. M. 2006a. Molecular marker and DNA sequencing methods. Pages 347369. in Motley, T.J., Cross, H., eds. Darwin's Harvest. New York Columbia University Press.CrossRefGoogle Scholar
Ward, S. M. 2006b. Genetic analysis of invasive plant populations at different spatial scales. Biol. Invasions 8:541552.Google Scholar
Ward, S. M., Reid, S. D., Harrington, J., Sutton, J., and Beck, K. G. 2006. Genetic diversity within and among invasive populations of yellow toadflax. Pages 4. in. Proceedings of the Annual Meeting of the Western Society of Weed Science. Las Cruces, NM Western Society of Weed Science.Google Scholar
Warwick, S. L. 1990. Genetic variation in weeds—with particular reference to Canadian agricultural weeds. Pages 318. in Kawano, S., ed. Biological Approaches and Evolutionary Trends in Plants. Boston Academic Press. 417.Google Scholar
Whitney, K. D., Randell, R. A., and Rieseberg, L. H. 2006. Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus . Am. Nat. 167:794807.Google Scholar
Williams, D. A., Overholt, W. A., Cuda, J. P., and Hughes, C. R. 2005. Chloroplast and micorosatellite DNA diversities reveal the introduction history of Brazilian peppertree (Schinus terebinthifolius) in Florida. Mol. Ecol. 14:36433656.Google Scholar
Williamson, M. H. and Fitter, A. 1996. The characters of successful invaders. Biol. Conserv. 78:163170.Google Scholar
Willis, A. J. and Blossey, B. 1999. Benign environments do not explain the increased vigour of non-indigenous plants: a cross-continental transplant experiment. Biocontrol Sci. Technol. 9:567577.Google Scholar
Willis, A. J., Memmott, J., and Forrester, R. I. 2000. Is there evidence for the post-invasion evolution of increased size among invasive plant species? Ecol. Lett. 3:275283.Google Scholar
Wilson, L. M., Ferher, J., Brautigam, S., and Grosskopf, G. 2006. A new invasive hawkweed (Hieracium sp.) in the Pacific Northwest. Can. J. Bot. 84:133142.Google Scholar
Ye, W-H., Mu, H-P., Cao, H-L., and Ge, X-J. 2003. Genetic structure of the invasive Chromolaena odorata in China. Weed Res. 44:129135.Google Scholar
Zhao, R., Cheng, Z., Lu, W., and Lu, B. 2006. Estimating genetic diversity and sampling strategy for a wild soybean (Glycine soja) population based on different molecular markers. Chinese Sci. Bull. 51:12191227.Google Scholar