Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-10T14:48:00.317Z Has data issue: false hasContentIssue false
  • English
  • Français

Microsatellites Uncover Multiple Introductions of Clonal Giant Reed (Arundo donax)

Published online by Cambridge University Press:  20 January 2017

Daniel Tarin ,
Alan E. Pepper ,
John A. Goolsby ,
Patrick J. Moran ,
Alberto Contreras Arquieta ,
Alan E. Kirk  and
James R. Manhart
Daniel Tarin*
Affiliation:
Texas A&M University, Department of Biology, College Station, TX 77843
Alan E. Pepper
Affiliation:
Texas A&M University, Department of Biology, College Station, TX 77843
John A. Goolsby
Affiliation:
U.S. Department of Agriculture, Agricultural Research Service, Kika de la Garza Subtropical Agricultural Research Center, Weslaco, TX 78596
Patrick J. Moran
Affiliation:
U.S. Department of Agriculture, Agricultural Research Service, Kika de la Garza Subtropical Agricultural Research Center, Weslaco, TX 78596
Alberto Contreras Arquieta
Affiliation:
Pronatura Norestre, Monterrey, Mexico
Alan E. Kirk
Affiliation:
USDA-ARS, European Biological Control Laboratory, Montpelier, France
James R. Manhart
Affiliation:
Texas A&M University, Department of Biology, College Station, TX 77843
*
Corresponding author's E-mail: dtarin@bio.tamu.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Giant reed (Arundo donax) is an invasive weed that is native to the Old World. Tens of thousands of hectares of riparian habitat in the Rio Grande Basin (RGB) in Texas and Mexico have been heavily affected by invasions of Arundo. Additionally, many other watersheds across the southwestern United States have also been affected. Giant reed is being targeted for biological control because it displaces native vegetation and consumes water that could potentially be used for agricultural and municipal purposes, especially in areas with limited access to water. Finding the best-adapted insects for biological control involves locating the origin(s) of this plant. To narrow down the proximal source(s) of invasion of giant reed in the RGB, 10 microsatellite markers were developed. An analysis of 203 Old World and 159 North American plants, with an emphasis on the RGB, indicated a reduction in the allelic diversity in the introduced range compared with the Old World. Clonal assignment, neighbor joining, principal coordinates analyses, and STRUCTURE analyses were consistent and implied multiple introductions in North America, with one (likely clonal) lineage responsible for the invasion of the RGB, northern Mexico, and other parts of the southwestern United States. Although no identical matches with the RGB lineage were found in the Old World, several close matches were found on the Mediterranean coast of Spain.

Keywords

Giant reed, Arundo donax L.Biological controlclonalinvasive speciesMediterraneanRio Grande BasinRGB
Type
Research
Information
Invasive Plant Science and Management , Volume 6 , Issue 3 , September 2013 , pp. 328 - 338
Copyright
Copyright © 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.)

References

Literature Cited

Ahmad, R., Liow, P. S., Spencer, D. F., and Jasieniuk, M. 2008. Molecular evidence for a single genetic clone of invasive Arundo donax in the United States. Aquat. Bot. 88:113–120.CrossRefGoogle Scholar
Arnaud-Haond, S., Duarte, C. M., Alberto, F., and Serrão, E. A. 2007. Standardizing methods to address clonality in population studies. Mol. Ecol. 16:5115–5135.CrossRefGoogle ScholarPubMed
Avise, J. C. 2004. Molecular Markers, Natural History, and Evolution. Sunderland, MA Sinauer Associates. 684 p.Google Scholar
Bell, G. 1997. Ecology and management of Arundo donax, and approaches to riparian habitat restoration in Southern California. Pages 103–113 in Brock, J. H., Wade, M., Pycek, P., and Green, D., eds. Plant Invasions: Studies from North America and Europe. Leiden, The Netherlands Blackhuys. Pp. 103–113.Google Scholar
Bhanwra, R. K., Choda, S. P., and Kumar, S. 1982. Comparative embryology of some grasses. Proc. Indian Acad. Sci. B Biol. Sci. 48:152–162.Google Scholar
Boland, J. M. 2006. The importance of layering in the rapid spread of Arundo donax (giant reed). Madroño 53:303–312.Google Scholar
Cloutier, D., Rioux, D., Beaulieu, J., and Schoen, D. J. 2003. Somatic stability of microsatellite loci in eastern white pine, Pinus strobus L. Heredity 90:247–252.Google Scholar
Connor, H. E. and Dawson, M. I. 1993. Evolution of reproduction in Lamprothyrsus (Arundineae: Gramineae). Ann. Mo. Bot. Gard. 80:512–517.Google Scholar
Dewoody, J., Nason, J. D., and Hipkins, V. D. 2006. Mitigating scoring errors in microsatellite data from wild populations. Mol. Ecol. Notes 6:951–957.CrossRefGoogle Scholar
Douhovnikoff, V. and Dodd, R. S. 2003. Intra-clonal variation and a similarity threshold for identification of clones: application to Salix exigua using AFLP molecular markers. Theor. Appl. Genet. 106:1307–1315.CrossRefGoogle Scholar
Dudley, T. L. 2000. Arundo donax L. Pages 53–58 in Bossard, C. C., Randall, J. M., and Hoshovsky, M. C., eds. Invasive Plants of California's Wildlands. Berkeley, CA University of California Press.Google Scholar
Dunmire, W. W. 2004. Gardens of New Spain: How Mediterranean Plants and Foods Changed America. Austin, TX University of Texas Press. 395 p.Google Scholar
Estoup, A. and Guillemaud, T. 2010. Restructuring routes of invasions using genetic data: why, how, and so what? Mol. Ecol. 19:4113–4130.Google Scholar
Evanno, G., Regnaut, S., and Goudet, J. 2005. Detecting the number of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14:2611–2620.Google Scholar
Everitt, J. H., Yang, C., and DeLoach, C. J. 2005. Remote sensing of giant reed with 7 QuickBird satellite imagery. J. Aquat. Plant Manage. 43:81–84.Google Scholar
Falush, D., Stephens, M., and Pritchard, J. K. 2003. Inference of population structure using multilocusdata: linked loci and correlated allele frequencies. Genetics 164:1567–1587.Google Scholar
Falush, D., Stephens, M., and Pritchard, J. K. 2007. Inference of population structure using multilocusdata: dominant markers and null alleles. Mol. Ecol. Notes 7:574–578.CrossRefGoogle ScholarPubMed
Frandsen, P. R. 1996. Team Arundo: interagency cooperation to control giant cane (Arundo donax). Pages 244–305 in Luken, J. O., and Thieret, J. W., eds. Assessment and Management of Plant Invasions. New York Springer-Verlag.Google Scholar
Garcia-Rossi, D., Rank, N., and Strong, D. R. 2003. Potential for self-defeating biological control? Variation in herbivore vulnerability among invasive Spartina genotypes. Ecol. Appl. 13:1640–1649.Google Scholar
Ginot, F. D. R., Bordelais, I., Nguyen, S., and Gyapay, G. 1996. Correction of some genotyping errors in automated fluorescent microsatellite analysis by enzymatic removal of one base overhangs. Nucleic Acids Res. 24:540–541.CrossRefGoogle ScholarPubMed
Goolsby, J. and Moran, P. J. 2009. Host range of Tetramesa romana Walker (Hymenoptera: Eurytomidae), a potential biological control of giant reed, Arundo donax L. in North America. Biol. Control 49:160–168.CrossRefGoogle Scholar
Goolsby, J. A., DeBarro, P. J., Makinson, J. R., Pemberton, R. W., Hartley, D. M., and Frohlich, D. 2006a. Matching the origin of an invasive weed for selection of a herbivore haplotype for a biological control programme. Mol. Ecol. 15:287–297.Google Scholar
Goolsby, J. A., Moran, P. J., Adamczyk, J. A., Kirk, A. A., Jones, W. A., Marcos, M. A., and Cortés, E. 2009. Host range of the European, rhizome-stem feeding scale Rhizaspidiotus donacis (Leonardi) (Hemiptera: Diaspididae), a candidate biological control agent for giant reed, Arundo donax L. (Poales: Poaceae) in North America. BioControl Sci. Technol. 19:899–918.Google Scholar
Goolsby, J. A., van Klinken, R. D., and Palmer, W. A. 2006b. Maximising the contribution of native-range studies towards the identification and prioritization of weed biocontrol agents. Aust. J. Entomol. 45:276–286.Google Scholar
Gould, F. W. and Shaw, R. B. 1983. Grass Systematics. College Station, TX Texas A&M University Press. 412 p.Google Scholar
Herrera, A. M. and Dudley, T. L. 2003. Reduction of riparian arthropod abundance and diversity as a consequence of giant reed (Arundo donax) invasion. Biol. Invasions 5:167–277.Google Scholar
Hubisz, M. J., Falush, D., Stephens, M., and Pritchard, J. K. 2009. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Res. 9:1322–1332.Google Scholar
Khudamrongsawat, J., Tayyar, R., and Holt, J. S. 2004. Genetic diversity of giant reed (Arundo donax) in the Santa Ana River, California. Weed Sci. 52:395–405.CrossRefGoogle Scholar
Lewandowski, I., Scurlock, J. M. O., Lindvall, E., and Christou, M. 2003. The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe. Biomass Bioenergy 25:335–361.CrossRefGoogle Scholar
Lian, C., Oishi, R., Miyashita, N., and Hogetsu, T. 2004. High somatic instability of a microsatellite locus in a clonal tree, Robinia pseudoacacia . Theor. Appl. Genet. 108:836–841.CrossRefGoogle Scholar
Lowe, S., Browne, M., Boudjelas, S., and De Poorter, M. 2000. 100 of the World's Worst Invasive Alien Species. A selection from the Global Invasive Species Database. Published by The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN). 12 p.Google Scholar
Mariani, C., Cabrini, R., Danin, A., Piffanelli, P., Fricano, A., Gomarasca, S., Dicandilo, M., Grassi, F., and Soave, C. 2010. Origin, diffusion, and reproduction of the giant reed (Arundo donax L.): a promising weedy energy crop. Ann. Appl. Biol. 157:191–202.CrossRefGoogle Scholar
McGaugh, S., Hendrickson, D., Bell, G., Cabral, H., McEachron, L., and Munoz, O. J. 2007. Fighting an Aggressive Wetlands Invader: A Case Study of Giant Reed (Arundo donax) and Its Threat to Cuatro Cienegas, Coahuila, Mexico. http://desertfishes.org/cuatroc/organisms/non-native/arundo/Arundo.html. Accessed January 1, 2013.Google Scholar
Meirmans, P. G. and Van Tienderen, P. H. 2004. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 4:792–794.Google Scholar
Mes, T. H. M., Kuperus, P., Kirschner, J., Stepánek, J., Storchová, H., Oosterveld, P., and Den Nijs, J. C. M. 2002. Detection of genetically divergent clone mates in apomictic dandelions. Mol. Ecol. 11:253–265.Google Scholar
Moran, P. J. and Goolsby, J. 2010a. Biology of the armored scale Rhizaspidiotus donacis (Hemiptera: Diaspididae), a candidate agent for biological control of giant reed (Arundo donax). Ann. Entomol. Soc. Am. 103:252–263.CrossRefGoogle Scholar
Moran, P. J. and Goolsby, J. 2010b. Biology of the galling wasp Tetramesa romana, a biological control agent of giant reed. Biol. Control 49:169–179.Google Scholar
O'Connell, L. M. and Ritland, K. 2004. Somatic mutations at microsatellite loci in western redcedar (Thuja plicata: Cupressaceae). J. Hered. 95:172–176.CrossRefGoogle ScholarPubMed
Paradis, E., Claude, J., and Strimmer, K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290.CrossRefGoogle ScholarPubMed
Pepper, A. E. and Norwood, L. E. 2001. Evolution of Caulanthus amplexicaulis var. barbarae (Brassicaceae), a rare serpentine endemic plant: A molecular phylogenetic perspective. Am. J. Bot. 88:1479–1489.Google Scholar
Perdue, R. E. 1958. Arundo donax—source of musical reeds and industrial cellulose. Econ. Bot. 12:368–404.Google Scholar
Pompanon, F., Bonin, A., Bellemain, E., and Taberlet, P. 2005. Genotyping errors: causes, consequences and solutions. Nat. Rev. Genet. 6:847–846.Google Scholar
Pritchard, J. K., Stephens, M., and Donnelly, P. J. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945–959.Google Scholar
R Development Core Team. 2009. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org. Accessed July 12, 2011.Google Scholar
Rogstad, S. H., Keane, B., and Beresh, J. 2002. Genetic variation across VTNR loci in central North American Taraxacum surveyed at different spatial scales. Plant Ecol. 1:111–121.Google Scholar
Saltonstall, K. 2003. Microsatellite variation within and among North American lineages of Phragmites australis . Mol. Ecol. 12:1689–1702.Google Scholar
Scott, G. 1993. Fire threat from Arundo donax . Pages 17–18 in Arundo donax workshop proceedings, Jackson, N. E., Frandsen, P., and Douthit, S. (eds). Ontario, CA.Google Scholar
Sharma, K. P., Kushwaha, SPS., and Gopal, B. 1998. A comparative study of stand structure and standing crops of two wetland species, Arundo donax and Phragmites karka, and primary production in Arundo donax with observations on the effect of clipping. Trop. Ecol. 39:3–14.Google Scholar
Terry, M., Pepper, A. E., and Manhart, J. R. 2006. Development and characterization of microsatellite loci in endangered Astrophytum asterias (Cactaceae). Mol. Ecol. Notes 6:865–866.Google Scholar
Thuillet, A.-C., Bru, D., David, J., Roumet, P., Santoni, S., Sourdille, P., and Bataillon, T. 2002. Direct estimation of mutation rate for 10 microsatellite loci in durum wheat, Triticum turgidum (L.) Thell. ssp durum . Mol. Biol. Evol. 19:122–125.CrossRefGoogle ScholarPubMed
Tracy, J. L. and DeLoach, C. J. 1998. Suitability of Classical Biological Control for Giant Reed (Arundo donax) in the United States. Pages 73–110 in Arundo and Saltcedar Management Workshop Proceedings. Ontario, California University of California Cooperative Extension, Holtville, California.Google Scholar
Udupa, S. and Baum, M. 2001. High mutation rate and mutational bias at (TAA)n microsatellite loci in chickpea (Cicer arietinum L.). MGG Mol. Genet. Genomics. 265:1097–1103.CrossRefGoogle ScholarPubMed
Vigouroux, Y., McMullen, M., Hittinger, C. T., Houchins, K., Schulz, L., Kresovich, S., Matsuoka, Y., and Doebley, J. 2002. Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. Proc. Natl. Acad. Sci. U. S. A. 99:9650–9655.Google Scholar
Weber, D. J. 1994. The Spanish Frontier in North America. New Haven, CT Yale University Press. 602 p.Google Scholar
Weising, K., Nybom, H., Wolff, K., and Kahl, G. 2005. DNA Fingerprinting in Plants: Principles, Methods, and Applications. Boca Raton, FL CRC Press. 472 p.Google Scholar