Skip to main content

Advertisement

SpringerLink
Log in

Disentangling the dynamics of invasive fireweed (Senecio madagascariensis Poir. species complex) in the Hawaiian Islands

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Studies investigating the genetic variation of invasive species render opportunities to better understand the dynamics of biological invasions from an ecological and evolutionary perspective. In this study, we investigate fine-scale population genetic structure of invasive Senecio madagascariensis (fireweed) using microsatellite markers to determine levels of genetic diversity and how it pertains to introduction history of this species within and among the Hawaiian Islands. Dispersal patterns were interpreted and, together with a habitat suitability analysis, we aim to describe the potential range expansion of S. madgascariensis within the islands. Bayesian and frequency-based analyses revealed genetic structure with two major genetic demes corresponding to the two fireweed-infested islands of Maui and Hawaii. Both these demes showed further genetic sub-structure, each consisting of three genetically distinct subgroups. Overall, fireweed showed significant levels of inbreeding. Major genetic demes (Maui and Hawaii) differed in observed heterozygosities, inbreeding and genetic structure, each harbouring a large proportion of private alleles. In contrast to the current understanding of fireweed’s introduction history between the Hawaiian Islands, fine-scale population genetic parameters suggest that this species has been introduced at least twice, possibly even more, to the archipelago. Spatial analyses also revealed high correlation between genetic similarity and geographical proximity (>2 km apart) followed by a sharp decline. In addition, a single population was identified that likely resulted from a rare human- or animal-mediated extreme long-distance dispersal event from Maui to Hawaii. Bayesian and likelihood estimates of ‘first generation migrants’ also concurred that contemporary dispersal occurs more frequently over smaller spatial scales than larger scales. These findings indicate that spread in this species occurs primarily via a stratified strategy. Predictions from habitat suitability models indicate all Hawaiian Islands as highly suitable for fireweed invasion and the movement of propagules to currently uninfested islands and outlying suitable habitats should be avoided to circumvent further expansions of the invasion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Amsellem L, Noyer JL, Le Bourgeois T, 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 9:443–455

    Article  CAS  PubMed  Google Scholar 

  • Barrett SCH, Colautti RI, Eckert CG (2008) Reproductive systems and evolution during biological invasion. Mol Ecol 17:373–383

    Article  PubMed  Google Scholar 

  • Beyer H (2006) Hawths analysis tools for ArcGIS, p. Spatial Ecology toolset extension for ArcGIS. Available at http://www.spatialecology.com/htools

  • Bjorkland MJ, Baker AJ (1996) The successful founder: genetics of introduced Carduelis chloris (greenfinch) populations in New Zealand. Heredity 77:410–422

    Article  Google Scholar 

  • Bonham-Carter GF (1994) Geographic information systems for geoscientists: modelling with GIS. Pergamon, Oxford

    Google Scholar 

  • Clevenger APJ, Wierzchowski J, Chruszcz B, Gunson K (2002) GIS-generated, expert-based models for identifying wildlife habitat linkages and planning mitigation passages. Conserv Biol 16:503–514

    Article  Google Scholar 

  • Coulon A, Fitzpatrick JW, Bowman R, Stith BM, Makarewich CA, Stenzler LM, Lovette IJ (2008) Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub-jay (Aphelocoma coerulescens). Mol Ecol 17:1685–1701

    Article  CAS  PubMed  Google Scholar 

  • Daly C, Halbleib M (2006) Pacifc Islands (Hawaii) average monthly and annual precipitation, 1971–2000 p. Raster digital format. The PRISM Group at Oregon State University, Corvallis, Oregon, USA

  • Daly C, Halbleib M (2006) Pacifc Islands (Hawaii) average monthly and annual minimum and maximum temperature and mean dewpoint temperature, 1971–2000 p. Raster digital format. The PRISM Group at Oregon State University, Corvallis, Oregon, USA

  • Durka W, Bossdorf O, Prati D, Auge H (2005) Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America. Mol Ecol 14:1697–1706

    Article  PubMed  Google Scholar 

  • EPA (1998) Land use and landcover of main Hawaiian Islands as of 1976, p. 1976 Digital GIRAS (Geographic information retrieval and analysis) files. State of Hawaii

  • Ernst WHO (1998) Invasion, dispersal and ecology of the South African neophyte Senecio inaequidens in The Netherlands: from wool alien to railway and road alien. Acta Bot Neerl 47:131–151

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances amomng DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    Article  CAS  PubMed  Google Scholar 

  • Gardner DR, Thorne MS, Molyneux RJ, Pfister JA, Seawright AA (2006) Pyrrolizidine alkaloids in Senecio madagascariensis from Australia and Hawaii and assessment of possible livestock poisoning. Biochem Syst Ecol 34:736–744

    Article  CAS  Google Scholar 

  • Goolsby JA, De Barro PJ, Makinson JR, Pemberton RW, Hartley DM, Frohlicj DR (2006) Matching the origin of an invasive weed for the selection of a herbivore haplotype for a biological control programme. Mol Ecol 16:287–297

    Article  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices version 2.9.3. Available from http://www.unil.ch/izea/softwares/fstat.html

  • Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186

    Article  Google Scholar 

  • Guo SW, Thompson EA (1992) A monte carlo method for combined segregation and linkage analysis. Am J Hum Genet 51:1111–1126

    CAS  PubMed  Google Scholar 

  • Hawaii Statewide GIS Program, Office of Planning, Department of Business, Economic Development & Tourism, Honolulu, Hawaii, USA. Available at http://hawaii.gov/dbedt/gis/

  • Hulme PE (2003) Biological invasions: winning the science battles but losing the conservation war? Oryx 37:178–193

    Article  Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6: 13. v.3.15 http://ibdws.sdsu.edu/

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kearney MR, Porter WP (2009) Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecol Lett 12:334–350

    Article  PubMed  Google Scholar 

  • Lafuma L, Maurice S (2007) Increase in mate availability without loss of self-incompatibility in the invasive species Senecio inaequidens (Asteraceae). Oikos 116:201–208

    Article  Google Scholar 

  • Lavergne S, Molofsky J (2007) Increased genetic diversity and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888

    Article  CAS  PubMed  Google Scholar 

  • Le Roux JJ, Wieczorek AM (2006) Isolation and characterization of polymorphic microsatellite markers from fireweed, Senecio madagascariensis Poir. (Asteraceae). Mol Ecol Notes 7:327–329

    Article  Google Scholar 

  • Le Roux J, Wieczorek AM (2009) Molecular systematics and population genetics of biological invasions: towards a better understanding of invasive species management. Ann Appl Biol 154:1–17

    Article  CAS  Google Scholar 

  • Le Roux JJ, Wieczorek AM, Ramadan MM, Tran CT (2006) The native provenance of invasive fireweed (Senecio madagascariensis Poir.) in the Hawaiian Islands as inferred from phylogenetic analysis. Divers Distrib 12:694–702

    Article  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Lenton SM, Fa JE, Perez Del Val J (2000) A simple non-parametric GIS model for predicting species distribution: endemic birds in Bioko Island, West Africa. Biodivers Conserv 9:869–885

    Article  Google Scholar 

  • Lyford ME, Jackson ST, Betancourt JL, Gray ST (2003) Influence of landscape structure and climate variability on a late Holocene plant migration. Ecol Monogr 73:567–583

    Article  Google Scholar 

  • Moody ME, Mack RN (1988) Controlling the spread of plant invasions: the importance of nascent foci. J Appl Ecol 25:1009–1021

    Article  Google Scholar 

  • Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:5446–5451

    Article  CAS  PubMed  Google Scholar 

  • Motooka P, Nagai G, Onuma K, DuPonte M, Kawabata A, Fukumoto G (1999) Control of fireweed (Senecio madagascariensis).CTAHR Publication on Weed Control WC-2. University of Hawaii Press, Honolulu

    Google Scholar 

  • Neuffer B, Hurka H (1999) Colonization history and introduction dynamics of Capsella bursa-pastoris (Brassicaceae) in North America: isozymes and quantitative traits. Mol Ecol 8:1667–1681

    Article  PubMed  Google Scholar 

  • NOAA (2000) Main eight Hawaiian islands land cover. National Oceanic and Atmospheric Administration, Coastal Services Center NOAA Coastal Services Center, Charleston, South Carolina

  • NOAA, NOS, NOAA/Biogeography Program (2001) Digital elevation models main Hawaiian Islands, National Oceanic and Atmospheric Administration, Center for Coastal Monitoring and Assessment, Silver Spring, Maryland

  • Novak SJ, Welfley AY (1997) Genetic diversity in the introduced clonal grass Poa bulbosa (Bulbous bluegrass). Northwest Sci 71:271–280

    Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57:1182–1195

    PubMed  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    Article  CAS  PubMed  Google Scholar 

  • Robertson BC, Gemmell NJ (2004) Defining eradication units in pest control programmes. J Appl Ecol 41:1042–1048

    Article  Google Scholar 

  • Rosenthal DM, Ramakrishnan AP, Cruzan MB (2008) Evidence for multiple sources of invasion and intraspecific hybridization in Brachypodium sylvaticum (Hudson) Beauv. in North America. Mol Ecol 17:4657–4669

    Article  PubMed  Google Scholar 

  • Rowe ML, Lee DJ, Nissen SJ, Bowditch BM, Masters RA (1997) Genetic variation in North American leafy spurge (Euphorbia esula) determined by DNA markers. Weed Sci 45:446–454

    CAS  Google Scholar 

  • Sakai AK, Weller SG, Allendorf FW, Holt JS, Lodge DM, Molofsky J et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN Version 2.000: a software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland

    Google Scholar 

  • Scott LJ, Congdon BC, Playford J (1998) Molecular evidence that fireweed (Senecio madagascariensis, Asteraceae) is of South African origin. Plant Syst Evol 213:251–257

    Article  Google Scholar 

  • Sindel BM, Michael PW (1988) Survey of the impact and control of fireweed (Senecio madagascariensis Poir.) in New South Wales. Plant Prot Q 13:22–28

    Google Scholar 

  • Sindel BM, Radford IJ, Holtkamp RH, Michael PW (1998) Senecio madagascariensis Poir. The biology of Australian weeds. 33. Plant Prot Q 13:2–15

    Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multi-allele and multilocus genetic structure. Heredity 82:561–573

    Article  PubMed  Google Scholar 

  • Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:354–371

    Article  Google Scholar 

  • van Kleunen M, Fischer M, Johnson SD (2007) Reproductive assurance through self-fertilization does not vary with population size in the alien invasive plant Datura stramonium. Oikos 116:1400–1412

    Article  Google Scholar 

  • Viard F, Ellien C, Dupont L (2006) Dispersal ability and invasion success of Crepidula fornicata in a single gulf: insights from genetic markers and larval-dispersal model. Helgol Mar Res 60:144–152

    Article  Google Scholar 

  • Vitousek PM (1990) Biological invasions and ecosystem processes: towards an integration of population biology and ecosystem studies. Oikos 57:7–13

    Article  Google Scholar 

  • Waltman S, Grantham K, Oman D, Muehlbach G (2002) Major land resource areas, p. Major Land Resource Areas for the main hawaiian islands. US Department of Agriculture (USDA) and Natural Resources Conservation Service (NRCS)

  • Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24:136–144

    Article  PubMed  Google Scholar 

  • Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420

    Article  Google Scholar 

  • Young AG, Murray BG (2000) Genetic bottlenecks and dysgenic gene flow into re-established populations of the grassland daisy, Rutidosis leptorrhynhoides. Aust J Bot 43:409–416

    Article  Google Scholar 

Download references

Acknowledgments

The following people provided valuable insights on previous drafts of this manuscript: Núria Roura-Pascual, Mark Wright, Daniel Rubinoff, and Curtis Daehler. The authors would also like to thank two anonymous reviewers for their constructive comments. This work was supported by a Tropical Subtropical Agriculture Research (TSTAR) United States Department of Agriculture, Cooperative State Research, Education, and Extension Service (USDA CREES) grand awarded to A.M.W.

Author information

Authors and Affiliations

  1. Department of Tropical Plant and Soil Sciences, University of Hawaii at Manoa, 3190 Maile Way, St. John 102, Honolulu, HI, 96822, USA

    Johannes J. Le Roux, Ania M. Wieczorek & Carol T. Tran

  2. Department of Botany and Zoology, Centre of Excellence for Invasion Biology, Stellenbosch University, Natural Sciences Building, Matieland, 7602, South Africa

    Johannes J. Le Roux

  3. Department of Plant and Environmental Protection Sciences, University of Hawaii at Manoa, 3050 Maile Way, Gilmore 310, Honolulu, HI, 96822, USA

    Adam E. Vorsino

Authors
  1. Johannes J. Le Roux
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ania M. Wieczorek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carol T. Tran
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Adam E. Vorsino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Johannes J. Le Roux.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 336 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Le Roux, J.J., Wieczorek, A.M., Tran, C.T. et al. Disentangling the dynamics of invasive fireweed (Senecio madagascariensis Poir. species complex) in the Hawaiian Islands. Biol Invasions 12, 2251–2264 (2010). https://doi.org/10.1007/s10530-009-9635-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-009-9635-9

Keywords

Search

Navigation