Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-12-05T11:16:05.878Z Has data issue: false hasContentIssue false

High genetic diversity in the clonal aquatic weed Alternanthera philoxeroides in the United States

Published online by Cambridge University Press:  04 November 2020

Dean A. Williams*
Affiliation:
Professor, Department of Biology, Texas Christian University, Fort Worth, TX, USA
Nathan E. Harms
Affiliation:
Research Biologist, Aquatic Ecology and Invasive Species Branch, Environmental Laboratory, U.S. Army Engineer Research and Development Center, Vicksburg, MS, USA
Ian A. Knight
Affiliation:
Postdoctoral Research Participant, Oak Ridge Institute for Science and Education, Oak Ridge, TN, USA
Brenda J. Grewell
Affiliation:
Research Ecologist, U.S. Department of Agriculture, Agricultural Research Service, Invasive Species and Pollinator Health Research Unit, Davis, CA, USA
Caryn Joy Futrell
Affiliation:
Biological Sciences Technician, U.S. Department of Agriculture, Agricultural Research Service, Invasive Species and Pollinator Health Research Unit, Davis, CA95616, USA
Paul D. Pratt
Affiliation:
Research Leader and Entomologist, U.S. Department of Agriculture, Agricultural Research Service, Invasive Species and Pollinator Health Research Unit, Albany, CA, USA
*
Author for correspondence: Dean A. Williams, Department of Biology, Texas Christian University, Fort Worth, TX76129. (Email: dean.williams@tcu.edu)

Abstract

The distribution of genetic diversity in invasive plant populations can have important management implications. Alligatorweed [Alternanthera philoxeroides (Mart.) Griseb.] was introduced into the United States around 1900 and has since spread throughout much of the southern United States and California. A successful biological control program was initiated in the late 1960s that reduced A. philoxeroides in the southern United States, although control has varied geographically. The degree to which variation among genotypes may be responsible for variation in control efficacy has not been well studied due to a lack of genetic data. We sampled 373 plants from 90 sites across the United States and genotyped all samples at three chloroplast regions to help inform future management efforts. Consistent with clonal spread, there was high differentiation between sites, yet we found six haplotypes and high haplotype diversity (mean h = 0.48) across states, suggesting this plant has been introduced multiple times. Two of the haplotypes correspond to previously described biotypes that differ in their susceptibility to herbicides and herbivory. The geographic distribution of the three common haplotypes varied by latitude and longitude, while the other haplotypes were widespread or localized to one or a few sites. All the haplotypes we screened are hexaploid (6n = 102), which may enhance biological control. Future studies can use these genetic data to determine whether genotypes differ in their invasiveness or respond differently to control measures. Some states, for instance, have mainly a single haplotype that may respond more uniformly to a single control strategy, whereas other states may require a variety of control strategies. These data will also provide the basis for identifying the source regions in South America, which may lead to the discovery of new biological control agents more closely matched to particular genotypes.

Type
Research Article
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of the Weed Science Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Associate Editor: Marie Jasieniuk, University of California, Davis

References

Benjamini, Y, Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289300 Google Scholar
Benoit, LK, Les, DH (2013) Rapid identification and molecular characterization of phytoene desaturase mutations in fluridone-resistant hydrilla (Hydrilla verticillata). Weed Sci 61:3240 CrossRefGoogle Scholar
Buckingham, GR (2002) 1 Alligatorweed. Pages 515 in Driesche, RV, Blossey, B, Hoddle, M, Lyon, S, Reardon, R, eds. Biological Control of Invasive Plants in the Eastern United States. Morgantown, WV: USDA Forest Service Publication FHTET-2002-04 Google Scholar
Bultemeier, BW, Netherland, MD, Ferrell, JA, Haller, WT (2009) Differential herbicide response among three phenotypes of Cabomba caroliniana . Invasive Plant Sci Manag 2:352359 CrossRefGoogle Scholar
Burnham, KP, Anderson, DR (2003) Model Selection and Multimodal Inference: A Practical Information-theoretic Approach. New York: Springer Science & Business Media. 488 pGoogle Scholar
Cai, H, Wei, CL, Chen, N (2009) Chromosome karyotype characters of biological invasion in Alternanthera philoxeroides . Chin J Tropical Crops 30:530534 Google Scholar
Chen, Z, Xiong, Z, Pan, X, Shen, S, Geng, Y, Xu, C, Chen, J, Zhang, W (2015) Variation of genome size and the ribosomal DNA ITS region of Alternanthera philoxeroides (Amaranthaceae) in Argentina, the USA, and China. J Syst Evol 53:8287 CrossRefGoogle Scholar
Clement, M, Posada, D, Crandall, KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:16571659 CrossRefGoogle ScholarPubMed
Cofrancesco, AF Jr (1988) Alligatorweed Survey of Ten Southern States. Miscellaneous Paper A-88-3. Vicksburg, MS: U.S. Army Engineer Waterways Experiment Station. 115 pGoogle Scholar
Coulson, JR (1977) Biological Control of Alligatorweed, 1959–1972. A Review and Evaluation. Washington, DC: USDA Technical Bulletin 1547. 98 pGoogle Scholar
Croxton, MD, Andreu, MA, Williams, DA, Overholt, WA, Smith, JA (2011) Geographic origins and genetic diversity of air-potato (Dioscorea bulbifera) in Florida. Invasive Plant Sci Manag 4:2230 CrossRefGoogle Scholar
Cuda, JP, Christ, LR, Manrique, V, Overholt, WA, Wheeler, GS, Williams, DA (2012) Role of molecular genetics in identifying “fine tuned” natural enemies of the invasive Brazilian peppertree, Schinus terebinthifolius: a review. Biocontrol 57:227233 CrossRefGoogle Scholar
Gaskin, JF, Bon, M-C, Cock, MJW, Cristofaro, M, De Biase, A, De Clerck-Floate, R, Ellison, CA, Hinz, HL, Hufbauer, RA, Julian, MH, Sforza, R (2011) Applying molecular-based approaches to classical biological control of weeds. Biol Control 58:121 CrossRefGoogle Scholar
Geng, Y, Pan, X, Xu, C, Zhang, W, Li, B, Chen, J, Lu, B, Song, Z (2007) Phenotypic plasticity rather than locally adapted ecotypes allows the invasive alligator weed to colonize a wide range of habitats. Biol Invasions 9:245256 CrossRefGoogle Scholar
Geng, Y, van Klinken, RD, Sosa, A, Li, B, Chen, J, Xu, C (2016) The relative importance of genetic diversity and phenotypic plasticity in determining invasion success of a clonal weed in the USA and China. Front Plant Sci 7:213 CrossRefGoogle ScholarPubMed
Grodowitz, M, Nachtrieb, J, Harms, N, Freedman, J (2010) Suitability of Using Introduced Hydrellia spp. for Management of Monoecious Hydrilla verticillata (Lf) Royle. Vicksburg, MS: U.S. Army Engineer Research and Development Center. 14 p CrossRefGoogle Scholar
Harms, NE, Cronin, JT (2020) Biological control agent attack timing and population variability, but not density, best explain target weed density across an environmental gradient. Sci Rep 10:11062 CrossRefGoogle Scholar
Jacono, CC, Richerson, MM, Howard Morgan, V, Pfingsten, IA (2020) Hydrilla verticillata (L.f.) Royle. Gainesville, FL: U.S. Geological Survey, Nonindigenous Aquatic Species Database. https://nas.er.usgs.gov/queries/FactSheet.aspx?SpeciesID=6. Revision date: February 3, 2020, peer review date: October 27, 2015Google Scholar
Kay, SH (1992) Response of two alligatorweed biotypes to Quinclorac. J Aquat Plant Manag 30:3540 Google Scholar
Kay, SH, Haller, WT (1982) Evidence for the existence of distinct alligatorweed biotypes. J Aquat Plant Manag 20:3741 Google Scholar
Kriticos, DJ, Jarošik, V, Ota, N (2014) Extending the suite of bioclim variables: a proposed registry system and case study using principal components analysis. Methods Ecol Evol 5:956960 CrossRefGoogle Scholar
Krug, P, Sosa, AJ (2019) Mother knows best: plant polyploidy affects feeding and oviposition preference of the alligator weed biological control agent, Agasicles hygrophila . Biocontrol 64:623632 CrossRefGoogle Scholar
LaRue, EA, Grimm, D, Thum, RA (2013) Laboratory crosses and genetic analysis of natural populations demonstrate sexual viability of invasive hybrid watermilfoils (Myriophyllum spicatum x M. sibiricum). Aquat Bot 109:4953 CrossRefGoogle Scholar
Leigh, JW, Bryant, D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:11101116 CrossRefGoogle Scholar
Liu, M, Zhou, F, Pan, X, Zhang, Z, Traw, MB, Li, B (2018) Specificity of herbivore-induced responses in an invasive species, Alternanthera philoxeroides (alligator weed). Ecol Evol 8:5970 CrossRefGoogle Scholar
Liu, W, Deng, R, Liu, W, Wang, Z, Ye, W, Wang, L, Cao, H, Shen, H (2011) Phenotypic differentiation is associated with gender plasticity and its responsive delay to environmental changes in Alternanthera philoxeroides - phenotypic differentiation in alligator weed. PLoS ONE 6:e27238 CrossRefGoogle ScholarPubMed
Madeira, PT, Coetzee, JA, Center, TD, White, EE, Tipping, PW (2007) The origin of Hydrilla verticillata recently discovered at a South African dam. Aquat Bot 87:176180 CrossRefGoogle Scholar
Manrique, V, Cuda, JP, Overholt, WA, Williams, DA, Wheeler, GS (2008) Effect of host-plant genotypes on the performance of three candidate biological control agents of Schinus terebinthifolius in Florida. Biol Control 47:167171 CrossRefGoogle Scholar
Michel, A, Arias, RS, Scheffler, BE, Duke, SO, Netherland, M, Dayan, FE (2004) Somatic mutation-mediated evolution of herbicide resistance in the nonindigenous invasive plant hydrilla (Hydrilla verticillata). Mol Ecol 13:32293237 CrossRefGoogle Scholar
Mukherjee, A, Williams, D, Gitzendanner, MA, Overholt, WA, Cuda, JP (2016) Microsatellite and chloroplast DNA diversity of the invasive aquatic weed Hygrophila polysperma in native and invasive ranges. Aquat Bot 129:5561 CrossRefGoogle Scholar
Netherland, MD, Jones, D (2015) Fluridone-resistant hydrilla (Hydrilla verticillata) is still dominant in the Kissimmee Chain of Lakes, FL. Invasive Plant Sci Manag 8:212218 CrossRefGoogle Scholar
Pan, XY, Jia, X, Fu, DJ, Li, B (2013) Geographical diversification of growth-defense strategies in an invasive plant. J Syst Evol 51:308317 CrossRefGoogle Scholar
Pandit, MK, White, SM, Pocock, MJO (2014) The contrasting effects of genome size, chromosome number and ploidy level on plant invasiveness: a global analysis. New Phytol 203:697703 CrossRefGoogle ScholarPubMed
Peakall, R, Smouse, PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288295 CrossRefGoogle Scholar
Peakall, R, Smouse, PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:25372539 CrossRefGoogle ScholarPubMed
R Core Team (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org Google Scholar
Sainty, G, McCorkelle, G, Julien, M (1998) Control and spread of alligator weed Alternanthera philoxeroides (Mart.) Griseb. in Australia: lessons for other regions. Wetl Ecol Manag 5:195201 CrossRefGoogle Scholar
Schaal, BA, Gaskin, JF, Caicedo, AL (2003) Phylogeography, haplotype trees and invasive plant species. J Hered 94:197204 CrossRefGoogle ScholarPubMed
Shaw, J, Lickey, EB, Beck, JT, Farmer, SB, Liu, W, Miller, J, Siripun, KC, Winder, CT, Schilling, EE, Small, RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142166.CrossRefGoogle ScholarPubMed
Sosa, AJ, Greizerstein, E, Cardo, MV, Telesnick, MC, Julien, MH (2008) The evolutionary history of an invasive species: alligator weed, Alternanthera philoxeroide. Pages 435442 in Julien MH, Sforza R, Bon MC, Evans HC, Hatcher PE, eds. Proceedings of the XII International Symposium on Biological Control of Weeds. Wallingford, UK: CAB InternationalGoogle Scholar
Sosa, AJ, Julien, MH, Cordo, HA (2004) New research on alligator weed (Alternanthera philoxeroides) in its South American native range. Pages 180185 in Cullen JM, Briese DT, Kriticos DJ, Lonsdale WM, Morin L, Scott JK, eds. Proceedings of the XI International Symposium on Biological Control of Weeds. Canberra, Australia: CSIRO EntomologyGoogle Scholar
Spencer, NR, Coulson, JR (1976) The biological control of alligatorweed Alternanthera philoxeroides in the USA. Aquat Bot 2:177190 CrossRefGoogle Scholar
Suda, J, Meyerson, LA, Leitch, IJ, Pysek, P (2015) The hidden side of plant invasions: the role of genome size. New Phytol 205:9941007 CrossRefGoogle ScholarPubMed
te Beest, M, Le Roux, JJ, Richardson, DM, Brysting, AK, Suda, J, Kubesova, M, Pysek, P (2012) The more the better? The role of polyploidy in facilitating plant invasions. Ann Bot 109:1945 CrossRefGoogle ScholarPubMed
Telesnicki, MC, Sosa, AJ, Greizerstein, E, Julien, MH (2011) Cytogenetic effect of Alternanthera philoxeroides (alligatorweed) on Agasicles hygrophila (Coleoptera: Chrysomelidae) in its native range. Biol Control 57:138142 CrossRefGoogle Scholar
Templeton, AR, Crandall, KA, Sing, CF (1992) A cladistic-analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. 3. Cladogram estimation. Genetics 132:619633 CrossRefGoogle Scholar
Thayer, DD, Pfingsten, IA (2020). Alternanthera philoxeroides (Mart.) Griseb. Gainesville, FL: U.S. Geological Survey, Nonindigenous Aquatic Species Database. https://nas.er.usgs.gov/queries/FactSheet.aspx?SpeciesID=227. Accessed: May 20, 2020Google Scholar
Thum, RA, Chorak, GM, Newman, RM, Eltawely, JA, Latimore, J, Elgin, E, Parks, S (2020) Genetic diversity and differentiation in populations of invasive Eurasian (Myriophyllyum spicatum) and hybrid (M. spicatum × M. sibiricum) watermilfoil. Invasive Plant Sci Manag 13:5967 CrossRefGoogle Scholar
Thum, RA, Wcisel, DJ, Zuellig, MP, Heilman, M, Hausler, P, Tyning, P, Huberty, L, Netherland, MD (2012) Field documentation of decreased herbicide response by a hybrid watermilfoil population. J Aquat Plant Manag 50:141146 Google Scholar
Tippery, NP, Bugbee, GJ, Stebbins, SE (2020) Evidence for a genetically distinct strain of introduced Hydrilla verticillata (Hydrocharitaceae) in North America. J Aquat Plant Manag 58:16 Google Scholar
Wain, RP, Haller, WT, Martin, DF (1984) Genetic relationship among two forms of alligatorweed. J Aquat Plant Manag 22:104105 Google Scholar
Ward, SM, Gaskin, JF, Wilson, LM (2008) Ecological genetics of plant invasion: what do we know? Invasive Plant Sci Manag 1:98109 CrossRefGoogle Scholar
Williams, DA, Harms, NE, Grodowitz, MJ, Purcell, M (2018) Genetic structure of Hydrilla verticillata L.f. Royle in eastern China and the Republic of Korea: implications for surveys of biological control agents for the invasive monoecious biotype. Aquat Bot 149:1727 CrossRefGoogle 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 14:36433656 CrossRefGoogle Scholar
Williams, WI, Friedman, JM, Gaskin, JF, Norton, AP (2014) Hybridization of an invasive shrub affects tolerance and resistance to defoliation by a biological control agent. Evol Appl 7:381393 CrossRefGoogle ScholarPubMed
Ye, WH, Li, J, Cao, HL, Ge, XJ (2003) Genetic uniformity of Alternanthera philoxeroides in south China. Weed Res 43:297302 CrossRefGoogle Scholar
Zeiger, CF (1967) Biological control of alligatorweed with Agasicles n. sp. in Florida. Hyacinth Control Journal 6:3134 Google Scholar
Zhang, Z, Zhou, F, Pan, X, van Kleunen, M, Liu, M, Li, B (2019) Evolution of increased intraspecific competitive ability following introduction: the importance of relatedness among genotypes. J Ecol 107:387395 CrossRefGoogle Scholar