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Morphological and phytochemical variation, genetic structure and phenology in an introgressive hybrid swarm of Senecio hercynicus and S. ovatus (Compositae, Senecioneae)

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Abstract

Introgressive hybridisation between Senecio hercynicus and Senecio ovatus (Compositae, Senecioneae) was studied in a mixed stand of the two species on the S- and SW-facing slopes of the German part of the Bohemian Forest (SE Germany). Morphological variation based on multivariate analysis of 14 diagnostic characters, along with genetic data from an amplified fragment length polymorphism (AFLP) fingerprinting analysis, indicates that the surveyed stand forms an intensively introgressed hybrid swarm. The majority of individuals were found to be intermediate between the two parental taxa, and strong statistical correlation between phenetic and genetic distances was observed. In contrast to that, flowering time of individuals (expressed as the time when 50% of the capitula of a plant were in flower) was found to follow a bimodal distribution in the hybrid swarm and lacked any correlation with the genetic and morphological relationships among plants. The same was true for the spectra of pyrrolizidine alkaloids (PA) revealed by a gas-chromatographic survey: most of the 142 individuals surveyed fell into one of two main chemotypes, only a few plants exhibited an intermediate and additive PA spectrum, and no correlation with the genetic and morphological relationships among plants was observed. Assuming that most of the AFLP markers are neutral, we conclude that the correlation of morphology with the genetic pattern may argue for the neutrality of morphological features analysed. Consequently, we interpret the lack of correlation between phenological and phytochemical data with the neutral genetic markers as evidence that both phenology and phytochemistry may be either under selection or that these features are genetically or biosynthetically constrained.

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References

  • Aldridge G, Campbell DR (2009) Genetic and morphological patterns show variation in frequency of hybrids between Ipomopsis (Polemoniaceae) zones of sympatry. Heredity 102:257–265

    Article  CAS  PubMed  Google Scholar 

  • Anderson E (1948) Hybridization of the habitat. Evolution 2:1–9

    Article  Google Scholar 

  • Anderson E (1949) Introgressive hybridization. Wiley, New York

    Google Scholar 

  • Antonovics J (2006) Evolution in closely adjacent plant populations: long-term persistence of prereproductive isolation at a mine boundary. Heredity 97:33–37

    Article  CAS  PubMed  Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Barton N, Hewitt G (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148

    Article  Google Scholar 

  • Buerkle CA, Lexer C (2008) Admixture as the basis for genetic mapping. Trends Ecol Evol 23:686–694

    Article  PubMed  Google Scholar 

  • Campbell D (2004) Natural selection in Ipomopsis hybrid zones: implications for ecological speciation. New Phytol 161:83–90

    Article  Google Scholar 

  • Campbell D, Waser N (2001) Genotype-by-environment interaction and the fitness of plant hybrids in the wild. Evolution 55:669–676

    Article  CAS  PubMed  Google Scholar 

  • Cheeke PR (1988) Toxicity and metabolism of pyrrolizidine alkaloids. J Anim Sci 66:2343–2350

    CAS  PubMed  Google Scholar 

  • Clausen J, Keck DD, Hiesey WM (1940) Experimental studies on the nature of species. I. Effect of varied environments on western North America plants. Carnegie Institute of Washington, Washington, DC: Publ. 520

  • Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365

    Article  PubMed  Google Scholar 

  • Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland

    Google Scholar 

  • Czesak ME, Knee MJ, Gale RG, Bodach SD, Fritz RS (2004) Genetic architecture of resistance to aphids and mites in a willow hybrid system. Heredity 93:619–626

    Article  CAS  PubMed  Google Scholar 

  • De Boer NJ (1999) Pyrrolizidine alkaloid distribution in Senecio jacobaea minimizes losses to generalist feeding. Entomol Exp Appl 91:169–173

    Article  Google Scholar 

  • Dierschke H (1995) Phänologische und symphänologiche Artengruppen von Blütenpflanzen in Mitteleuropa. Tuexenia 15:523–560

    Google Scholar 

  • Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22:432–439

    Article  PubMed  Google Scholar 

  • Endler J (1977) Geographic variation, speciation, and clines. Princeton Univ Press, Princeton

    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 

  • Franks SJ, Sim S, Weis AE (2007) Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc Natl Acad Sci USA 104:1278–1284

    Article  CAS  PubMed  Google Scholar 

  • Fritz RS (1999) Resistance of hybrid plants to herbivores: genes, environment, or both? Ecology 80:382–391

    Article  Google Scholar 

  • Fritz RS, McDonough SE, Rhoads AG (1997) Effects of plant hybridization on herbivore–parasitoid interactions. Oecologia 110:360–367

    Article  Google Scholar 

  • Fritz RS, Moulia C, Newcombe G (1999) Resistance of hybrid plants and animals to herbivores, pathogens, and parasites. Annu Rev Ecol Syst 30:565–591

    Article  Google Scholar 

  • Grabherr G, Gottfried M, Pauli H (1994) Climate effects on mountain plants. Nature 369:448

    Article  Google Scholar 

  • Grant V (1971) Plant speciation. Columbia University Press, New York

    Google Scholar 

  • Graumann S, Gottsberger G (1988) Reproductive strategies in allogamous and autogamous Senecio species. Lagascalia 15(Extra):673–679

    Google Scholar 

  • Hagen J (2003) Genetisch und modifikativ bedingte Variabilität der Pyrrolizidinalkaloide in Senecio jacobea L. Thesis, Technische Universität Braunschweig

  • Hartmann T, Toppel G (1987) Senecionine N-oxide, the primary product of pyrrolizidine alkaloid biosynthesis in root cultures of Senecio vulgaris. Phytochemistry 26:1639–1643

    Article  CAS  Google Scholar 

  • Herborg J (1987) Die Variabilität und Sippenabgrenzung in der Senecio nemorensis-Gruppe (Compositae) im europäischen Teilareal. Diss Bot 107:1–262

    Google Scholar 

  • Herrera CM, Bazaga P (2008) Population-genomic approach reveals adaptive floral divergence in discrete populations of hawk moth-pollinated violet. Mol Ecol 17:5378–5390

    Article  CAS  PubMed  Google Scholar 

  • Hochwender CG, Fritz RS, Orians CM (2000) Using hybrid systems to explore the evolution of tolerance to damage. Evol Ecol 14:509–521

    Article  Google Scholar 

  • Hodálová I (1996) Sympatric populations of Senecio ovatus subsp. ovatus, S. germanicus subsp. germanicus (Compositae) and their hybrid in the Carpathians and the adjacent part of Pannonia. I. Multivariate morphometric study. Flora 191:283–290

    Google Scholar 

  • Hodálová I (1999) Multivariate analysis of the Senecio nemorensis group (Compositae) in the Carpathians with a new species from the east Carpathians. Folia Geobot 34:321–335

    Article  Google Scholar 

  • Hodálová I (2002) A new hybrid Senecio × slovacus from the S. nemorensis group (Compositae) in the West Carpathians. Biologia 57:75–82

    Google Scholar 

  • Hol WHG, van Veen JA (2002) Pyrrolizidine alkaloids from Senecio jacobaea affect fungal growth. J Chem Ecol 28:1763–1772

    Article  CAS  PubMed  Google Scholar 

  • Jiggins CD, Mallet J (2000) Bimodal hybrid zones and speciation. Trends Ecol Evol 15:250–255

    Article  PubMed  Google Scholar 

  • Kirk H, Máčel M, Klinkhamer GL, Vrieling K (2004) Natural hybridisation between Senecio jacobaea and Senecio aquaticus: molecular and chemical evidence. Mol Ecol 13:2267–2274

    Article  CAS  PubMed  Google Scholar 

  • Konechnaja G (1979) De generis Senecio L. specibus partis europaeae URSS. 1. Sectio Pseudo-oliganthi Sof. Novosti Sistematiki Vysshikh Rastenii 15:216–219

    Google Scholar 

  • Kovach WL (1999) MVSP: a multivariate statistical package for windows, version 3.1. Kovach Computing Services, Pentraeth

    Google Scholar 

  • Lenoir J, Gégout JC, Marquet PA, de Ruffray P, Brisse H (2008) A significant upward shift in plant species optimum elevation during the 20th century. Science 320:1768–1771

    Article  CAS  PubMed  Google Scholar 

  • Lotsy JP (1925) Species or Linneon. Genetica 7:487–506

    Article  Google Scholar 

  • Lotsy JP (1931) On the species of the taxonomist in its relation to evolution. Genetica 13:1–16

    Article  Google Scholar 

  • Macel M, Klinkhamer PGL, Vrieling K, van der Meijden E (2002) Diversity of pyrrolizidine alkaloids in Senecio species does not affect the specialist herbivore Tyria jacobaeae. Oecologia 133:541–550

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • McCune B, Mefford MJ (1999) Multivariate analysis of ecological data, version 4.10. MjM Software, Gleneden Beach

    Google Scholar 

  • McNeilly T, Antonovic J (1968) Evolution in closely adjacent plant populations. IV. Barriers to gene flow. Heredity 23:205–218

    Article  Google Scholar 

  • Meister J, Hubaishan MA, Kilian N, Oberprieler C (2006) Temporal and spatial diversification of the shrub Justicia areysiana Deflers (Acanthaceae) endemic to the monsoon affected coastal mountains of the southern Arabian Peninsula. Plant Syst Evol 262:153–171

    Article  Google Scholar 

  • Meister J, Kilian N, Oberprieler C (2008) Genetic structure of Euclea schimperi (Ebenaceae) populations in monsoonal fog oases of the Southern Arabian Peninsula. Nord J Bot 25:217–226

    Article  Google Scholar 

  • Mitchell-Olds T, Schmitt J (2006) Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441:947–952

    Article  CAS  PubMed  Google Scholar 

  • Moccia MD, Widmer A, Cozzolino S (2007) The strength of reproductive isolation in two hybridizing food-deceptive orchid species. Mol Ecol 16:2855–2866

    Article  PubMed  Google Scholar 

  • Oberprieler C (1989) Numerisch-taxonomische Studien in bayerischen Populationen der Senecio nemorensis-Gruppe (Compositae). Thesis, Ludwig-Maximilians-University, Munich

  • Oberprieler C (1994) Die Senecio nemorensis-Gruppe (Compositae, Senecioneae) in Bayern. Berichte der Bayerischen Botanischen Gesellschaft 64:7–54

    Google Scholar 

  • Oberprieler C, Meister J, Schneider C, Kilian N (2009) Genetic structure of Anogeissus dhofarica (Combretaceae) populations endemic to the monsoonal fog oases of the southern Arabian Peninsula. Biol J Linn Soc 97:40–51

    Article  Google Scholar 

  • Orians CM (2000) The effects of hybridization in plants on secondary chemistry: implications for the ecology and evolution of plant–herbivore interactions. Am J Bot 87:1749–1756

    Article  CAS  PubMed  Google Scholar 

  • Orr HA (2005) The genetic theory of adaptation: a brief history. Nat Rev Genet 6:119–127

    Article  CAS  PubMed  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx V6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Pelser BP, de Vos H, Theuring C, Beuerle T, Vrieling K, Hartmann T (2005) Frequent gain and loss of pyrrolizidine alkaloids in the evolution of Senecio section Jacobaea (Asteraceae). Phytochemistry 66:1285–1295

    Article  CAS  PubMed  Google Scholar 

  • Pelser BP, Veldkamp J-F, van der Meijden R (2006) New combinations in Jacobaea Mill. (Asteraceae, Senecioneae). Compos Newsl 44:1–11

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Quinn JA, Wetherington JD (2002) Genetic variability and phenotypic plasticity in flowering phenology in populations of two grasses. J Torrey Bot Soc 129:96–106

    Article  Google Scholar 

  • Raudnitschka D, Hensen I, Oberprieler C (2007) Introgressive hybridisation of Senecio hercynicus and S. ovatus (Compositae, Senecioneae) along an altitudinal gradient in Hochharz National Park (Saxony-Anhalt, Germany). System Biodivers 5:333–344

    Article  Google Scholar 

  • Rieseberg LH, Wendel JF (1993) Introgression and its consequences in plants. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, Oxford, pp 70–109

    Google Scholar 

  • Rieseberg LH, Whitton J, Gardner K (1999) Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152:713–727

    CAS  PubMed  Google Scholar 

  • Riihimäki M, Savolainen O (2004) Environmental and genetic effects on flowering differences between northern and southern populations of Arabidopsis lyrata (Brassicaceae). Am J Bot 91:1036–1045

    Article  Google Scholar 

  • Scheidel U, Bruelheide H (2001) Altitudinal differences in herbivory on montane Compositae species. Oecologia 129:75–86

    Article  Google Scholar 

  • Sherry RA, Zhou X, Gu S, Ill JAA, Schimel DS, Verburg PS, Wallace LL, Luo Y (2007) Divergence of reproductive phenology under climate warming. Proc Natl Acad Sci USA 104:198–202

    Article  CAS  PubMed  Google Scholar 

  • Stebbins GL (1950) Variation and evolution in plants. Columbia University Press, New York

    Google Scholar 

  • Stinchcombe JR, Hoekstra HE (2008) Combining population genomics and quantitative genetics: finding genes underlying ecologically important traits. Heredity 100:158–170

    Article  CAS  PubMed  Google Scholar 

  • Truong C, Palmé AE, Felber F (2007) Recent invasion of the mountain birch Betula pubescens ssp. tortuosa above the treeline due to climate change: genetic and ecological study in northern Sweden. J Evol Biol 20:369–380

    Article  CAS  PubMed  Google Scholar 

  • Turesson G (1922) The genotypical response of the plant species to the habitats. Hereditas 3:211–350

    Article  Google Scholar 

  • Turesson G (1930) The selective effect of climate upon the plant species. Hereditas 14:99–152

    Google Scholar 

  • Vos P, Hogers R, Bleeker M et al (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acid Res 23:4407–4414

    Article  CAS  PubMed  Google Scholar 

  • Vrieling K, de Vos H, van Wijk CAM (1993) Genetic analysis of the concentrations of pyrrolizidine alkaloids in Senecio jacobaea. Phytochemistry 32:1141–1144

    Article  CAS  Google Scholar 

  • Witte L, Ernst L, Adam H, Hartmann T (1992) Chemotypes of two pyrrolizidine alkaloid-containing Senecio species. Phytochemistry 31:559–565

    Article  CAS  Google Scholar 

  • Witte L, Rubiolo P, Bicchi C, Hartmann T (1993) Comparative analysis of pyrrolizidine alkaloids from natural sources by gas chromatography–mass spectrometry. Phytochemistry 32:187–196

    Article  Google Scholar 

  • Wolfe LM, Elzinga JA, Biere A (2004) Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecol Lett 7:813–820

    Article  Google Scholar 

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Acknowledgments

We would like to thank Dr. J. Meister and Mr. P. Hummel for their technical support in the molecular laboratory of CO at the Institute of Botany at the University of Regensburg. The help of Dr. Till Beuerle (University of Braunschweig, Institute of Pharmaceutical Biology) is gratefully acknowledged for running GC–MS measurements of representative PA-enriched extracts as well as for very fruitful discussions. We thank Mrs. G. Brunner (University of Regensburg, Institute of Pharmaceutical Biology) for excellent technical assistance, Mr. J. Kiermaier (University of Regensburg, Zentrale Analytik, Chemistry and Pharmacy) for running GC–MS spectra and an anonymous reviewer who improved our contribution considerably.

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Correspondence to Christoph Oberprieler.

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A. Barth and S. Schwarz contributed equally to this study.

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Oberprieler, C., Barth, A., Schwarz, S. et al. Morphological and phytochemical variation, genetic structure and phenology in an introgressive hybrid swarm of Senecio hercynicus and S. ovatus (Compositae, Senecioneae). Plant Syst Evol 286, 153–166 (2010). https://doi.org/10.1007/s00606-010-0295-0

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