Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-28T17:28:24.739Z Has data issue: false hasContentIssue false

High phenotypic variation of seed traits, germination characteristics and genetic diversity of an invasive annual weed

Published online by Cambridge University Press:  10 January 2013

Lydia Hantsch*
Affiliation:
Institute of Biology, Geobotany and Botanical Garden, Martin-Luther-University Halle-Wittenberg, Germany
Helge Bruelheide
Affiliation:
Institute of Biology, Geobotany and Botanical Garden, Martin-Luther-University Halle-Wittenberg, Germany
Alexandra Erfmeier
Affiliation:
Institute of Biology, Geobotany and Botanical Garden, Martin-Luther-University Halle-Wittenberg, Germany
*
*Correspondence E-mail: [email protected]

Abstract

Both phenotypic and genetic variation can affect the establishment success of exotic species. Using the weed Senecio vernalis Waldst. & Kit. with a continuous westward expansion of the native geographic range, we asked to what degree seed traits and germination patterns differ among different habitat disturbance types in the introduced region. We hypothesized that seed traits and germination pattern differ between different disturbance types, with lighter seeds and enhanced germination speed in highly disturbed habitats. Since S. vernalis colonizes successfully various disturbed habitats, we expected to find a high phenotypic genetic variation. Individuals from 19 populations were sampled from one region in Eastern Germany to study seed trait variation and germination success by means of a germination experiment and to assess genetic patterns using amplified fragment length polymorphism (AFLP) markers. Contrary to our expectation, habitat disturbance types did not differ in seed traits, germination characteristics or genetic variation. Instead, we found highest phenotypic and genetic variation within populations. Maximum percentage of germination was positively affected by seed mass. In addition, there was a weak but significant association between AFLP band patterns and population size and seed width, indicating that some variation in seed traits has a genetic component. In conclusion, the absence of a population differentiation at this geographic scale makes it unlikely that adaptation to different disturbance regimes is involved. Instead, a high variation in seed traits, overall high germination and genetic variation within populations under a wide range of habitat disturbance conditions seems to enable the offspring to colonize various habitat disturbance types.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2013

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

Annapurna, C. and Singh, J.S. (2003) Variation of Parthenium hysterophorus in response to soil quality: implications for invasiveness. Weed Science 43, 190198.Google Scholar
Bachmann, U.andHensen, I. (2007) Is declining Campanula glomerata threatened by genetic factors? Plant Species Biology 22, 110.CrossRefGoogle Scholar
Baker, H.G. (1974) The evolution of weeds. Annual Review of Ecology and Systematics 5, 124.CrossRefGoogle Scholar
Beckmann, M., Bruelheide, H. and Erfmeier, A. (2011) Germination responses of three grassland species differ between native and invasive origins. Ecological Research 26, 763777.CrossRefGoogle Scholar
Bu, H., Chen, X., Xu, X., Liu, K., Jia, P. and Du, G. (2007) Seed mass and germination in an alpine meadow on the eastern Tsinghai-Tibet plateau. Plant Ecology 191, 127149.CrossRefGoogle Scholar
Buckley, Y.M., Downey, P., Fowler, S.V., Hill, R., Memmot, J., Norambuena, H., Pitcairn, M., Shaw, R., Sheppard, A.W., Winks, C., Wittenberg, R.andRees, M. (2003) Are invasives bigger? A global study of seed size variation in two invasive shrubs. Ecology 84, 14341440.CrossRefGoogle Scholar
Butola, J.S., Vashistha, R.K., Malik, A.R. and Samant, S.S. (2010) Assessment of inter-population variability in Heracleum candidans wall with emphasis on seed characteristics and germination behavior. Journal of Medicinal Plants Research 4, 15231534.Google Scholar
Caño, L., Escarré, J., Vrieling, K. and Sans, X. (2009) Palatability to a generalist herbivore, defence and growth of invasive and native Senecio species: testing the evolution of increased competitive ability hypothesis. Oecologia 159, 95106.CrossRefGoogle ScholarPubMed
Chamorro, L. and Sans, F.X. (2010) Life-history variation in agricultural and wild populations of Erucastrum nasturtiifolium (Brassicaceae). Flora 205, 2636.CrossRefGoogle Scholar
Colautti, R.I., Grigorovich, I.A. and MacIsaak, H.J. (2006) Propagule pressure: A null model for biological invasions. Biological Invasions 8, 10231037.CrossRefGoogle Scholar
Comes, H.P. (1995) Genecological and isozyme studies in Senecio vernalis Waldst. & Kit. and S. vulgaris L. var. vulgaris from Central Europe and Israel. Flora 190, 201224.CrossRefGoogle Scholar
Comes, H.P. and Abbott, R.J. (1998) The relative importance of historical events and gene flow on the population structure of a Mediterranean ragwort, Senecio gallicus (Asteraceae). Evolution 52, 355367.CrossRefGoogle ScholarPubMed
Comes, H.P. and Abbott, R.J. (1999) Population structure and gene flow across arid versus mesic environments: A comparative study of two parapatric Senecio species from the Near East. Evolution 53, 3654.CrossRefGoogle ScholarPubMed
Comes, H.P. and Kadereit, J.W. (1990) Aspects of hybridization between the closely related Senecio vulgaris L. and Senecio vernalis Waldst. & Kit. Flora 184, 381388.CrossRefGoogle Scholar
Comes, H.P. and Kadereit, J.W. (1996) Genetic basis of speed of development in Senecio vulgaris L. var. vulgaris, S. vulgaris ssp. denticulatus (O.F. Muell.) P.D. Sell, and Senecio vernalis Waldst. & Kit. Heredity 77, 544554.CrossRefGoogle Scholar
Crawford, K.M. and Whitney, K.D. (2010) Population genetic diversity influences colonization success. Molecular Ecology 19, 12531263.CrossRefGoogle ScholarPubMed
Davidson, A.M., Jennions, M.andNicotra, A.B. (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecology Letters 14, 419431.CrossRefGoogle ScholarPubMed
de Clavijo, E.R. (2002) Variation of Parthenium hysterophorus in response to soil quality: implications for invasiveness. Annals of Botany 90, 279286.Google Scholar
de Clavijo, E.R. and Jiménez, M. (1998) The influence of achene type and plant density on growth and biomass allocation in the heterocarpic annual Catanache lutea (Asteraceae). International Journal of Plant Sciences 159, 637647.CrossRefGoogle Scholar
Dlugosch, K.M. and Parker, I.M. (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17, 431449.CrossRefGoogle ScholarPubMed
Doorduin, L.J., van den Hof, K., Vrieling, K. and Joshi, J. (2010) The lack of genetic bottleneck in invasive Tansy ragwort populations suggests multiple source populations. Basic and Applied Ecology 11, 244250.CrossRefGoogle 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. Molecular Ecology 14, 16971706.CrossRefGoogle ScholarPubMed
Erfmeier, A., Böhnke, M. and Bruelheide, H. (2011) Secondary invasion of Acer negundo: the role of phenotypic responses versus local adaptation. Biological Invasions 13, 15991614.CrossRefGoogle Scholar
Eriksson, O. (1999) Seed size variation and its effect on germination and seedling performance in the clonal herb Convallaria majalis. Acta Oecologica 20, 6166.CrossRefGoogle Scholar
Faast, R., Facelli, J.M.andAustin, A.D. (2011) Seed viability in declining populations of Caladenia rigida (Orchidaceae): are small populations doomed? Plant Biology 13, 8695.CrossRefGoogle ScholarPubMed
Fumanal, B., Chauvel, B., Sabatier, A.andBretagnolle, F. (2007) Variability and cryptic heteromorphism of Ambrosia artemisiifolia seeds: what consequences for its invasion in France? Annals of Botany 100, 305311.CrossRefGoogle ScholarPubMed
Funk, J.L. (2008) Differences in plasticity between invasive and native plants from a low resource environment. Journal of Ecology 98, 11621173.CrossRefGoogle Scholar
Garcia-Serrano, H., Escarré, J. and Sans, F.X. (2008) Comparing the effect of habitat on the magnitude of inbreeding depression in the Mediterranean native Senecio malacitanus and the alien S. inaequidens: consequences for invasive ability. Botany 86, 6375.CrossRefGoogle Scholar
Gargano, D., Gullo, T.andBernardo, L. (2011) Do inefficient selfing and inbreeding depression challenge the persistence of the rare Dianthus guliae Janka (Caryophyllaceae)? Influence of reproductive traits on a plant's proneness to extinction. Plant Species Biology 24, 6976.CrossRefGoogle Scholar
Haldimann, P., Steinger, T. and Müller-Schärer, H. (2003) Low genetic differentiation among seasonal cohorts in Senecio vulgaris as revealed by amplified fragment length polymorphism analysis. Molecular Ecology 12, 25412551.CrossRefGoogle ScholarPubMed
Hao, J.-H., Qiang, S., Liu, Q.Q. and Cao, F. (2009) Reproductive traits associated with invasiveness in Conyza sumatrensis. Journal of Systematics and Evolution 47, 245254.CrossRefGoogle Scholar
Hedrick, P.W. (2005) Genetics of populations. Sudbury, Massachusetts, Jones and Bartlett Publishers.Google Scholar
Henry, P., Le Lay, G., Goudet, J., Guisan, A., Jahodová, S. and Besnard, G. (2009) Reduced genetic diversity, increased isolation and multiple introductions of invasive giant hogweed in the western Swiss Alps. Molecular Ecology 18, 28192831.CrossRefGoogle ScholarPubMed
Hulme, P. (2008) Phenotypic plasticity and plant invasions: is it all Jack? Functional Ecology 22, 37.CrossRefGoogle Scholar
Jacquemyn, H., Brys, R. and Hermy, M. (2001) Within and between plant variation in seed number, seed mass and germinability of Primula elatior: Effect of population size. Plant Biology 3, 561568.CrossRefGoogle Scholar
Joost, S., Bonin, A., Bruford, M.W., Després, S.L., Conord, C., Erhardt, G. and Taberlet, P. (2007) A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Molecular Ecology 16, 39553969.CrossRefGoogle ScholarPubMed
Joost, S., Kalbermatten, M. and Bonin, A. (2008) Spatial analysis method (SAM): a software tool combining molecular and environmental data to identify candidate loci for selection. Molecular Ecology Resource 8, 957960.CrossRefGoogle Scholar
Jorritsma-Wienk, L.D., Ameloot, E., Lenssen, J.P.M. and Kroon, H. (2006) Differential responses of germination and seedling establishment in populations of Tragopogon pratensis (Asteraceae). Plant Biology 9, 109115.CrossRefGoogle ScholarPubMed
Jurado, E. and Westoby, M. (1992) Seedling growth in relation to seed size among species of arid Australia. Journal of Ecology 80, 407416.CrossRefGoogle Scholar
Kang, H. and Primack, R.B. (1991) Temporal variation of flower and fruit size in relation to seed yield in Celandine Poppy (Chelidonium majus, Papaveraceae). American Journal of Botany 78, 711722.CrossRefGoogle Scholar
Klotz, S. and Kühn, I. (2002) Indikatoren zum anthropogenen Einfluss auf die Vegetation. BIOLFLOR – Eine Datenbank mit biologisch-ökologischen Merkmalen zur Flora von Deutschland. Bundesamt für Naturschutz.Google Scholar
Kolar, C. and Lodge, D.M. (2001) Progress in invasion biology: predicting invaders. Trends in Ecology & Evolution 16, 199204.CrossRefGoogle ScholarPubMed
Lachmuth, S., Durka, W. and Schurr, F. (2010) The making of a rapid plant invader: genetic diversity and differentiation in the native and invaded range of Senecio inaequidens. Molecular Ecology 19, 39523967.CrossRefGoogle ScholarPubMed
Lambrinos, J.G. (2002) The variable invasive success of Cortaderia species in a complex landscape. Ecology 83, 518529.CrossRefGoogle Scholar
Lavergne, S. and Molofsky, J. (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proceedings of the National Academy of Sciences, USA 104, 38833888.CrossRefGoogle ScholarPubMed
Lee, C.E. (2002) Evolutionary genetics of invasive species. Trends in Ecology & Evolution 17, 386391.CrossRefGoogle Scholar
Li, Y.-P. and Feng, Y.-L. (2009) Differences in seed morphometric and germination traits of crofton weed (Eupatorium adenophorum) from different elevations. Weed Science 57, 2630.CrossRefGoogle Scholar
Lockwood, J.L., Cassey, P. and Blackburn, T.M. (2009) The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Diversity and Distributions 15, 904910.CrossRefGoogle Scholar
Mandák, B., Zákravský, P., Korínková, D., Dostál, P. and Plačková, I. (2009) Low population differentiation and high genetic diversity in the invasive species Carduus acanthoides L. (Asteraceae) within its native range in the Czech Republic. Biological Journal of the Linnean Society 98, 596607.CrossRefGoogle Scholar
Mandák, B., Zákravský, P., Dostál, P. and Plačková, I. (2011) Population genetic structure of the noxious weed Amaranthus retroflexus in Central Europe. Flora 206, 697703.CrossRefGoogle Scholar
McIntyre, S., Lavorel, S. and Tremont, R.M. (1995) Plant life-history attributes: their relationship to disturbance response in herbaceous vegetation. Journal of Ecology 83, 3144.CrossRefGoogle Scholar
Meerts, P. and Garnier, E. (1996) Variation in relative growth rate and its components in the annual Polygonum aviculare in relation to habitat disturbance and seed size. Oecologia 108, 438445.CrossRefGoogle ScholarPubMed
Meusel, H. and Jäger, E.J. (1992) Vergleichende Chorologie der Zentraleuropäischen Flora III (Textteil). Jena, Fischer.Google Scholar
Michalski, S.G., Durka, W., Jentsch, A., Kreyling, J., Pompe, S., Schweiger, O., Willner, E. and Beierkuhnlein, C. (2010) Evidence for genetic differentiation and divergent selection in an autotetraploid forage grass (Arrhenatherum elatius). Theoretical and Applied Genetics 120, 11511162.CrossRefGoogle Scholar
Monty, A. and Mahy, G. (2010) Evolution of dispersal traits along an invasion route in the wind-dispersed Senecio inaequidens (Asteraceae). Oikos 119, 15631570.CrossRefGoogle Scholar
Müller-Schärer, H. and Fischer, M. (2001) Genetic structure of the annual weed Senecio vulgaris in relation to habitat type and population size. Molecular Ecology 10, 1728.CrossRefGoogle ScholarPubMed
Münzbergová, Z. and Plačková, I. (2010) Seed mass and population characteristics interact to determine performance of Scorzonera hispanica under common garden conditions. Flora – Morphology, Distribution, Functional Ecology of Plants 205, 552559.CrossRefGoogle Scholar
Obeso, J.R. (1993) Seed mass variation in the perennial herb Asphodelus albus: sources of variation and position effect. Oecologia 93, 571575.CrossRefGoogle ScholarPubMed
Oksanen, J., Kindt, R., Legendre, P. and O'Hara, B. (2006) Vegan: Community ecology package. Available from website:http://cc.oulu.fi/~jarioksa/softhelp/vegan.html (accessed accessed December 2012).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. Conservation Biology 17, 5972.CrossRefGoogle Scholar
Peakall, R. and Smouse, P.E. (2001) GenAlEx: Genetic analysis in Excel. Canberra, Australian National University. Available from website:http://www.anu.edu.au/BoZo/GenAlEx.Google Scholar
Pérez-Figueroa, A., García-Pereira, M.J., Saura, M., Rolán-Alvarez, E. and Caballero, A. (2010) Comparing three different methods to detect selective loci using dominant markers. Journal of Evolutionary Biology 23, 22672276.CrossRefGoogle ScholarPubMed
Pico, F.X., Ouborg, N.J. and Groenendael, J.N. (2003) Fitness traits and dispersal ability in the herb Tragopogon pratensis (Asteraceae): decoupling the role of inbreeding depression and maternal effects. Plant Biology 5, 522530.CrossRefGoogle Scholar
Prentis, P.J., White, E.M., Radford, I.J., Lowe, A.J.andClarke, A.R. (2007) Can hybridization cause local extinction: A case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis? New Phytologist 176, 902912.CrossRefGoogle ScholarPubMed
Qui, J., Fu, Y.B., Bai, Y.G. and Wilmshurst, J.F. (2009) Genetic variation in remnant Festuca hallii populations is weakly differentiated, but geographically associated across the Canadian Prairie. Plant Species Biology 24, 156168.Google Scholar
R Development Core Team (2008) R: A language and environment for statistical computing. Austria, Vienna, R Foundation for Statistical Computing.Google Scholar
Ramakrishan, A.P., Meyer, S.E., Fairbanks, D.J. and Coleman, C.E. (2006) Ecological significance of microsatellite variation in western North American populations of Bromus tectorum. Plant Species Biology 21, 6173.CrossRefGoogle Scholar
Richards, C.L., Bossdorf, O., Muth, N.Z., Gurevitch, J.andPigliucci, M. (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters 9, 981993.CrossRefGoogle ScholarPubMed
Sambatti, J.B.M. and Rice, K.J. (2006) Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis). Evolution 60, 696710.Google ScholarPubMed
Schubert, P., O'Neill, R., Kohler, W. and Waldhardt, R. (2002) Reproductive traits and genetic diversity of Arabidopsis thaliana populations originating from different agricultural regimes. Journal of Plant Diseases and Protection 18, 5766.Google Scholar
Shi, M.M., Michalski, S., Chen, X.-Y. and Durka, W. (2011) Isolation by elevation in a subtropical dominant tree. PlosOne 6, e21302.Google Scholar
Suding, K.N., Goldberg, D.E. and Hartman, K.M. (2003) Relationships among species traits: separating levels of response and identifying linkages to abundance. Ecology 84, 116.CrossRefGoogle Scholar
Vergeer, P., Sonderen, E. and Ouborg, N.J. (2004) Introduction strategies put to the test: local adaptation versus heterosis. Conservation Biology 18, 812821.CrossRefGoogle Scholar
Violle, C., Castro, H., Richarte, J.andNavas, M.-L. (2009) Intraspecific seed trait variations and competition: passive or adaptive response? Functional Ecology 23, 612620.CrossRefGoogle Scholar
Wagenitz, G. (1987) Illustrierte Flora von Mittel-Europa (Begr. G. Hegi), vol. VI/2 (2nd edition). München, Lehmann Verlag.Google Scholar
Williamson, M.H. and Fitter, A. (1996) The varying success of invaders. Ecology 77, 16611666.CrossRefGoogle Scholar
Supplementary material: File

Hantsch Supplementary Material

Appendix

Download Hantsch Supplementary Material(File)
File 26.1 KB
Supplementary material: Image

Hantsch Supplementary Material

Appendix

Download Hantsch Supplementary Material(Image)
Image 40.7 KB
Supplementary material: File

Hantsch Supplementary Material

Appendix

Download Hantsch Supplementary Material(File)
File 34.3 KB