Plant Systematics and Evolution

, Volume 293, Issue 1–4, pp 177–191 | Cite as

Morphological, phytochemical and genetic variation in mixed stands and a hybrid swarm of Senecio germanicus and S. ovatus (Compositae, Senecioneae)

  • Christoph Oberprieler
  • Sabine Hartl
  • Kerstin Schauer
  • Jörg Meister
  • Jörg Heilmann
Original Article

Abstract

Mixed stands of Senecio ovatus subsp. ovatus and S. germanicus subsp. germanicus occur in the colline belt of central and eastern Europe. The latter species is adapted to more continental climate conditions and shows a later flowering time (August–September) than the widespread S. ovatus (July–August) that grows in more oceanic climates. We have surveyed 253 plants from 15 populations north of Regensburg (south-eastern Germany) using 16 qualitative and quantitative morphological characters and molecular markers [amplified fragment length polymorphisms (AFLP)] to detect introgressive hybridisation between these two species. Both multivariate statistical analyses based on morphological characters and the Bayesian clustering based on AFLP fingerprint data show that in most populations under study the two species form distinct entities and do not hybridise with each other. However, in one population from the Upper Palatine Forest a high number of intermediate individuals were found. A more detailed genetic (AFLP) and phytochemical (pyrrolizidine alkaloid, PA) analysis based on 125 individuals from this hybrid swarm indicated that these intermediate individuals are backcrosses towards S.germanicus. It is shown that the two species differ considerably concerning the qualitative and quantitative PA patterns and that backcrossed individuals either show an additive PA pattern or a PA pattern similar to S.germanicus, while in quantitative respects all of these individuals are approaching S.germanicus. These findings are discussed in terms of differential selection regimes influencing the fitness of pure and hybrid plants in an area which is an eco-climatological optimum for the more oceanic S.ovatus but which forms a distributional edge for the more continental S.germanicus.

Keywords

AFLP fingerprinting Asteraceae Chemical defence Herbivory Hybridisation Introgression Pyrrolizidine alkaloids Senecio 

References

  1. Anderson E (1948) Hybridization of the habitat. Evolution 2:1–9CrossRefGoogle Scholar
  2. Anderson E (1949) Introgressive hybridization. Wiley, New YorkGoogle Scholar
  3. Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229PubMedGoogle Scholar
  4. Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, OxfordGoogle Scholar
  5. Barton N, Hewitt G (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148CrossRefGoogle Scholar
  6. Campbell D (2004) Natural selection in Ipompsis hybrid zones: implications for ecological speciation. New Phytol 161:83–90CrossRefGoogle Scholar
  7. Campbell D, Waser N (2001) Genotype-by-environment interaction and the fitness of plant hybrids in the wild. Evolution 55:669–676PubMedCrossRefGoogle Scholar
  8. Cheeke PR (1988) Toxicity and metabolism of pyrrolizidine alkaloids. J Anim Sci 66:2343–2350PubMedGoogle Scholar
  9. Coyne JA, Orr HA (2004) Speciation. Sinauer, SunderlandGoogle Scholar
  10. 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 93:619–626PubMedCrossRefGoogle Scholar
  11. De Boer NJ (1999) Pyrrolizidine alkaloid distribution in Senecio jacobaea rosettes minimizes losses to generalist feeding. Entomologia Exper Appl 91:169–173CrossRefGoogle Scholar
  12. Endler J (1977) Geographic variation, speciation, and clines. Princeton University Press, PrincetonGoogle Scholar
  13. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  14. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578PubMedCrossRefGoogle Scholar
  15. Fielding AH (2007) Cluster and classification techniques for the biosciences. Cambridge University Press, CambridgeGoogle Scholar
  16. Fritz RS (1999) Resistance of hybrid plants to herbivores: genes, environment, or both? Ecology 80:382–391CrossRefGoogle Scholar
  17. Fritz RS, McDonough SE, Rhoads AG (1997) Effects of plant hybridization on herbivore–parasitoid interactions. Oecologia 110:360–367CrossRefGoogle Scholar
  18. Fritz RS, Moulia C, Newcombe G (1999) Resistance of hybrid plants and animals to herbivores, pathogens, and parasites. Annu Rev Ecol Syst 30:565–591CrossRefGoogle Scholar
  19. Gower JC (1971) A general coefficient of similarities and some of its properties. Biometrics 27:857–871CrossRefGoogle Scholar
  20. Grant V (1971) Plant speciation. Columbia University Press, New YorkGoogle Scholar
  21. Hagen J (2003) Genetisch und modifikativ bedingte Variabilität der Pyrrolizidinalkaloide in Senecio jacobea L. PhD Thesis, Technische Universität Braunschweig, BraunschweigGoogle Scholar
  22. Hartmann T, Toppel G (1987) Senecionine N-oxide, the primary product of pyrrolizidine alkaloid biosynthesis in root cultures of Senecio vulgaris. Phytochemistry 26:1639–1643CrossRefGoogle Scholar
  23. Herborg J (1987) Die Variabilität und Sippenabgrenzung in der Senecio nemorensis-Gruppe (Compositae) im europäischen Teilareal. Diss Bot 107:1–262Google Scholar
  24. Hochwender CG, Fritz RS, Orians CM (2000) Using hybrid systems to explore the evolution of tolerance to damage. Evol Ecol 14:509–521CrossRefGoogle Scholar
  25. Hodálová I (1999) Multivariate analysis of the Senecio nemorensis group (Compositae) in the Carpathians with a new species from the east Carpathians. Folia Geobot 34:321–335CrossRefGoogle Scholar
  26. Hodálová I (2002) A new hybrid Senecio × slovacus from the S. nemorensis group (Compositae) in the West Carpathians. Biologia 57:75–82Google Scholar
  27. Hodálová I, Marhold K (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 191:283–290Google Scholar
  28. Hodálová I, Valachnovič M (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. II. Synecological differentiation and distribution. Flora 191:291–302Google Scholar
  29. Hol WHG, van Veen JA (2002) Pyrrolizidine alkaloids from Senecio jacobaea affect fungal growth. J Chem Ecol 28:1763–1772PubMedCrossRefGoogle Scholar
  30. Kirk H, Máčel M, Klinkhamer GL, Vrieling K (2004) Natural hybridisation between Senecio jacobaea and Senecio aquaticus: molecular and chemical evidence. Mol Ecol 13:2267–2274PubMedCrossRefGoogle Scholar
  31. Konechnaja G (1979) De generis Senecio L. specibus partis europaeae URSS. 1. Sectio Pseudo-oliganthi Sof. Novosti Sistematiki Vysshikh Rastenii 15:216–219Google Scholar
  32. Kovach WL (1999) MVSP—a multivariate statistical package for Windows, version 3.1. Kovach Computing Services, PentraethGoogle Scholar
  33. Kucowa I (1976) Zmieność Senecio nemorensis L ssp. nemorensis I ssp. fuchsii (Gmel.) Čelak. W zbiorowiskach leśnych południowej Polski. Fragmenta Florist Geobot 22:445–462Google Scholar
  34. Langel D, Ober D, Pleser PB (2010) The evolution of pyrrolizidine alkaloid biosynthesis and diversity in the Senecioneae. Phytochem Rev 9. doi:10.1007/s11101-010-9184-y
  35. Lotsy JP (1925) Species or linneon. Genetica 7:487–506CrossRefGoogle Scholar
  36. Lotsy JP (1931) On the species of the taxonomist in its relation to evolution. Genetica 13:1–16CrossRefGoogle Scholar
  37. 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 133:541–550CrossRefGoogle Scholar
  38. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  39. Martin NH, Bouck AC, Arnold ML (2005) Loci affecting long-term hybrid survivorship in Louisana irises: implications for reproductive isolation and introgression. Evolution 59:2116–2124PubMedGoogle Scholar
  40. McCune B, Mefford MJ (1999) Multivariate analysis of ecological data, version 4.10. MjM Software, Gleneden BeachGoogle Scholar
  41. 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 262:153–171CrossRefGoogle Scholar
  42. 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 25:217–226CrossRefGoogle Scholar
  43. Moccia MD, Widmer A, Cozzolino S (2007) The strength of reproductive isolation in two hybridizing food-deceptive orchid species. Mol Ecol 16:2855–2866PubMedCrossRefGoogle Scholar
  44. Oberprieler C (1989) Numerisch-taxonomische Studien in bayerischen Populationen der Senecio nemorensis-Gruppe (Compositae). Thesis, Ludwig-Maximilians-University, MunichGoogle Scholar
  45. Oberprieler C (1994) Die Senecio nemorensis-Gruppe (Compositae, Senecioneae) in Bayern. Ber Bayer Bot Ges 64:7–54Google Scholar
  46. Oberprieler C, Meister J, Schneider CH, 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 97:40–51CrossRefGoogle Scholar
  47. Oberprieler C, Barth A, Schwarz S, Heilmann J (2010) Morphological and phytochemical variation, genetic structure, and phenology in an introgressive hybrid swarm of Senecio hercynicus and S. ovatus (Compositae, Senecioneae). Plant Syst Evol 286:153–166Google Scholar
  48. 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 87:1749–1756PubMedCrossRefGoogle Scholar
  49. Orr HA (2005) The genetic theory of adaptation: a brief history. Nat Rev Genet 6:119–127PubMedCrossRefGoogle Scholar
  50. Peakall R, Smouse PE (2006) GenAlEx V6: genetic analysis in Excel population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  51. Pelser PB, 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 66:1285–1295PubMedCrossRefGoogle Scholar
  52. Pelser PB, Veldkamp J-F, van der Meijden R (2006) New combinations in Jacobaea Mill (Asteraceae, Senecioneae). Compos Newslett 44:1–11Google Scholar
  53. Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  54. 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). Syst Biodivers 5:333–344CrossRefGoogle Scholar
  55. 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 70–109Google Scholar
  56. Rieseberg LH, Whitton J, Gardner K (1999) Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152:713–727PubMedGoogle Scholar
  57. Schweitzer JA, Martinsen GD, Whithzam TG (2002) Cottonwood hybrids gain fitness traits of both parents: a mechanism for their long-term persistence? Am J Bot 89:981–990CrossRefGoogle Scholar
  58. Vos P, Hogers R, Bleeker M et al (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acid Res 23:4407–4414PubMedCrossRefGoogle Scholar
  59. Vrieling K, de Vos H, van Wijk CAM (1993) Genetic analysis of the concentrations of pyrrolizidine alkaloids in Senecio jacobaea. Phytochemistry 32:1141–1144CrossRefGoogle Scholar
  60. Witte L, Rubiolo P, Bicchi C, Hartmann T (1993) Comparative analysis of pyrrolizidine alkaloids from natural sources by gas chromatography-mass spectrometry. Phytochemistry 32:187–196CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Christoph Oberprieler
    • 1
  • Sabine Hartl
    • 1
  • Kerstin Schauer
    • 1
  • Jörg Meister
    • 1
  • Jörg Heilmann
    • 2
  1. 1.Institute of BotanyUniversity of RegensburgRegensburgGermany
  2. 2.Institute of PharmacyUniversity of RegensburgRegensburgGermany

Personalised recommendations