Advertisement

Biological Invasions

, Volume 11, Issue 5, pp 1175–1187 | Cite as

Tumbleweed (Salsola, section Kali) species and speciation in California

  • Debra Ayres
  • Frederick J. Ryan
  • Eva Grotkopp
  • John Bailey
  • John Gaskin
Original Paper

Abstract

Tumbleweeds (Salsola species, section Kali) are road side and rangeland pest plants throughout the 48 contiguous states in the US. Three described tumbleweed species and two undescribed Salsola taxa occur in California. The known species are Russian thistle, Salsola tragus, introduced from Eurasia in the 1800s, Russian barbwire thistle, S. paulsenii, which grows in the desert regions of California, and is also native to Eurasia, and the recently identified S. kali subspecies austroafricana, possibly native to South Africa. Our goals were to investigate karyology, genome size, and molecular genetic affinities of the described species and the other taxa within their ranges in California using recently developed microsatellite loci, dominant nuclear DNA markers (RAPD and ISSR), and DNA sequence data. Chromosome counts and genome size assessments made with flow cytometry were compared. These analyses indicated that one undescribed taxon is a new allopolyploid hybrid between S. tragus and S. kali subspecies austroafricana, and the other undescribed taxon appears to be a complex hybrid involving all three described species. The invasion potentials for the hybrid taxa are unknown. Tumbleweeds are the focus of biological controls efforts but the identification of suitable agents for the hybrid taxa may be problematic because of the large amount of genetic variability encompassed within this evolving Salsola complex.

Keywords

Allopolyploid speciation Invasive hybrids Salsola tragus 

Notes

Acknowledgments

We thank the University of California Integrated Pest Management Program for funding this project, Drs. Patrick Akers and Fred Hrusa of the California Department of Food and Agriculture for plant and seed collection, and Alex Lee for invaluable lab assistance.

References

  1. Aagaard SMD, Sastad SM, Greilhuber J, Moen A (2005) A secondary hybrid zone between diploid Dactylorhiza incarnata ssp cruenta and allotetraploid D. lapponica (Orchidaceae). Heredity 94:488–496CrossRefPubMedGoogle Scholar
  2. Abbott RJ, Lowe AJ (2004) Origins, establishment and evolution of new polyploid species: Senecio cambrensis and S. eboracensis in the British Isles. Biol J Linn Soc 82:467–474CrossRefGoogle Scholar
  3. Ainouche ML, Baumel A, Salmon A (2004) Spartina anglica C.E. Hubbard: a natural model system for analyzing early evolutionary changes that affect allopolyploid genomes. Biol J Linn Soc 83:475–484CrossRefGoogle Scholar
  4. Akers RP, Pitcairn MJ, Hrusa F, Ryan F (2002) Identification and mapping of Russian thistle (Salsola tragus) and its types. California Department of Food and Agriculture Annual Report. www.cdfa.ca.gov/phpps/ipc/biocontrol/annuals/2002annual/2002bc25_salsola.pdf
  5. Arnold HL (1972) An analysis of the taxonomic status of a new taxon in the genus Salsola. PhD Dissertation, Utah State University, LoganGoogle Scholar
  6. Ayres DR, Grotkopp E, Zaremba K, Sloop CM, Blum MJ, Bailey JP, Antilla CK, Strong DR (2008) Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA. Am J Bot 95:713–719CrossRefGoogle Scholar
  7. Beatley JC (1973) Russian thistle (Salsola) species in Western United States. J Range Manag 26:225–226CrossRefGoogle Scholar
  8. Bennett MD, Leitch IJ (2005) Plant DNA C-values database (release 4.0). http://www.kew.org/cval/homepage.html
  9. Borger CPD (2007) The biology and ecology of Salsola australis R.Br. (Chenopodiaceae) in southwest Australian cropping systems. Dissertation, University of Western Australia, PerthGoogle Scholar
  10. Bruckart W, Calvin C, Vajna L, Schwarczinger I, Ryan FJ (2004) Differential susceptibility of Russian thistle accessions to Colletotrichum gloeosporioides. Biol Control 30:306–311CrossRefGoogle Scholar
  11. Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846CrossRefPubMedGoogle Scholar
  12. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050CrossRefPubMedGoogle Scholar
  13. Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051CrossRefPubMedGoogle Scholar
  14. Gaskin JF, Ryan FJ, Hrusa GF, Londo JP (2006) The genotype diversity of Salsola tragus and potential origins of a previously unidentified invasive Salsola from California and Arizona. Madroño 53:246–253CrossRefGoogle Scholar
  15. Han F, Fedak G, Guo W, Liu B (2005) Rapid and repeatable elimination of a parental genome-specific DNA repeat (pGc1R–1a) in newly synthesized wheat allopolyploids. Genetics 170:1239–1245CrossRefPubMedGoogle Scholar
  16. Hawkes RB, Mayfield A (1978) Coleophora klimeschiella, biological control agent for Russian thistle: host specificity testing. Environ Entomol 7:257–261Google Scholar
  17. Johnston JS, Bennett MD, Rayburn AL, Galbraith DW, Price HJ (1999) Reference standards for determination of DNA content of plant nuclei. Am J Bot 86:609–613CrossRefPubMedGoogle Scholar
  18. Leitch IJ, Bennett MD (2004) Genome downsizing in polyploid plants. Biol J Linn Soc 82:651–663CrossRefGoogle Scholar
  19. Levy AA, Feldman M (2002) The impact of polyploidy on grass genome evolution. Plant Physiol 130:1587–1593CrossRefPubMedGoogle Scholar
  20. Masterson J (1994) Stomatal size in fossil plants–evidence for polyploidy in majority of angiosperms. Science 264:421–424CrossRefPubMedGoogle Scholar
  21. McGray HG, Ayres DR, Sloop CM, Lee AK (2007) Beta SSR loci cross-amplify in five Salsola taxa. Mol Ecol Res 8:608–611. doi:  10.1111/j.1471-8286.2007.02014.x CrossRefGoogle Scholar
  22. Mosyakin SL (1996) A taxonomic synopsis of the genus Salsola L. (Chenopodiaceae) in North America. Ann Mo Bot Gard 83:387–395CrossRefGoogle Scholar
  23. Mosyakin SL (2003) Salsola Linnaeus. In: Flora of North America Editorial Committee (eds) Flora of North America north of Mexico, Magnoliphyta, Caryophillidae, vol 4, Part 1. Oxford University Press, New York, pp 398–403Google Scholar
  24. Muller H, Nuessly GS, Goeden RD (1990) Natural enemies and host-plant asynchrony contributing to the failure of the introduced moth, Coleophora-parthenica meyrick (Lepidoptera, Coleophoridae), to control Russian thistle. Agric Ecosyst Environ 32:133–142CrossRefGoogle Scholar
  25. Munz PA (1968) Supplement to a California flora. University of California Press, Berkeley, p 75Google Scholar
  26. Pires JC, Lim KY, Kovarík A, Matyásek R, Boyd A, Leitch AR, Leitch IJ, Bennett MD, Soltis PS, Soltis DE (2004) Molecular cytogenetic analysis of recently evolved Tragopogon (Asteraceae) allopolyploids reveal a karyotype that is additive of the diploid progenitors. Am J Bot 91:1022–1035CrossRefGoogle Scholar
  27. Rambaut A (1996) Se-Al: sequence alignment editor. Available at http://evolve.zoo.ox.ac.uk/
  28. Rilke S (1999) Revision der Sektion Salsola s. l. der Gattung Salsola (Chenopodiaceae). Biblio Bot (Stuttgart) 149:1–190Google Scholar
  29. Rilke S, Reimann C (1996) Morphological and ecophysiological differences between the subspecies of Salsola kali L. in Europe: results of culture experiments. Flora 191:363–376Google Scholar
  30. Rohlf FJ (2000) NTSYS-pc numerical taxonomy and multivariate analysis system version 2.1 manual. Applied Biostatistics Inc., New YorkGoogle Scholar
  31. Ryan FJ, Ayres DR (2000) Molecular markers indicate two cryptic, genetically divergent populations of Russian thistle (Salsola tragus) in California. Can J Bot 78:59–67CrossRefGoogle Scholar
  32. Ryan FJ, Ayres DR, Bell DE (1999) There’s more to tumbleweed (Russian thistle) than meets the eye. In: Kelly M, Howe M, Neill B (eds) Proceedings of the California exotic pest plant council symposium, vol 5. pp 11–19Google Scholar
  33. Ryan FJ, Mosyakin SL, Pitcairn MJ (2007) Molecular comparisons of Salsola tragus from California and Ukraine. Can J Bot 85:224–229CrossRefGoogle Scholar
  34. Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14:1163–1175CrossRefPubMedGoogle Scholar
  35. Shinn CH (1895) The Russian thistle in California. University of California Agricultural Experiment Station Bulletin No. 107Google Scholar
  36. Skalická K, Lim KY, Matysek R, Matzke M, Leitch AR, Kovarik A (2005) Preferential elimination of repeated DNA sequences from the paternal, Nicotiana tomentosiformis genome donor of a synthetic, allotetraploid tobacco. New Phytol 166:291–303CrossRefPubMedGoogle Scholar
  37. Smith L (2005) Host plant specificity and potential impact of Aceria salsolae (Acari: Eriophyidae), an agent proposed for biological control of Russian thistle (Salsola tragus). Biol Control 34:83–92CrossRefGoogle Scholar
  38. Sobhian R, Fumanal B, Pitcairn MJ (2003a) Observations on the host specificity and biology of Lixus salsolae (Co., Curculionidae), a potential biological control agent of Russian thistle, Salsola tragus (Chenopodiaceae) in North America. J Appl Entomol 127:322–324CrossRefGoogle Scholar
  39. Sobhian R, Ryan FJ, Khamraev A, Pitcairn MJ, Bell DE (2003b) DNA phenotyping to find a natural enemy in Uzbekistan for California biotypes of Salsola tragus L. Biol Control 28:222–228. doi: 10.1016/S1049-9644(03)00068-9 CrossRefGoogle Scholar
  40. Vaio M, Mazzella C, Porro V, Speranza P, López-Carro B, Estramil E, Folle GA (2007) Nuclear DNA content in allopolyploid species and synthetic hybrids in the grass genus Paspalum. Plant Syst Evol 265:109–121CrossRefGoogle Scholar
  41. Wilken DH (1993) Salsola. In: Hickman JC (ed) The Jepson manual. University of California Press, Berkeley, p 514Google Scholar
  42. Young JA (1988) The public response to the catastrophic spread of Russian thistle (1880) and halogeton (1945). Agric Hist 62:122–130Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Debra Ayres
    • 1
  • Frederick J. Ryan
    • 2
  • Eva Grotkopp
    • 1
  • John Bailey
    • 3
  • John Gaskin
    • 4
  1. 1.Department of Evolution and EcologyUniversity of CaliforniaDavisUSA
  2. 2.FresnoUSA
  3. 3.Department of BiologyUniversity of LeicesterLeicesterUK
  4. 4.United States Department of Agriculture, Agricultural Research ServiceNorthern Plains Agricultural Research LaboratorySidneyUSA

Personalised recommendations