, Volume 107, Issue 3, pp 307–320 | Cite as

Host adaptation in the anther smut fungus Ustilago violacea (Microbotryum violaceum): infection success, spore production and alteration of floral traits on two host species and their F1-hybrid

  • Arjen Biere
  • Sonja Honders
Population Ecology


It is often assumed that host specialization is promoted by trade-offs in the performance of parasites on different host species, but experimental evidence for such trade-offs is scant. We studied differences in performance among strains of the anther smut fungus Ustilago violacea from two closely related host plant species, Silene alba and S. dioica, on progeny of (1) the host species from which they originated, (2) the alternative host species, and (3) inter-specific hybrids. Significant intra-specific variation in the pathogen was found for both infection success on a range of host genotypes (virulence) and components of spore production per infected host (aggressiveness) (sensu Burdon 1987). Strains did not have overall higher virulence on conspecifics of their host of origin than on strains from the heterospecific host, but they did have a significantly (c. 3 times) higher spore production per infected male host. This finding suggests that host adaptation may have evolved with respect to aggressiveness rather than virulence. The higher aggressiveness of strains on conspecifics of their host of origin resulted both from higher spore production per infected flower (spores are produced in the anthers), and greater ability to stimulate flower production on infected hosts. The latter indicates the presence of adaptive intraspecific variation in the ability of host manipulation. As transmission of the fungus is mediated by insects that are both pollinators of the host and vectors of the disease, we also assessed the effect of strains on host floral traits. Infection resulted in a reduction of inflorescence height, flower size, and nectar production per flower. Strains did not differ in their effect on nectar production, but infection with strains from S. alba resulted in a stronger reduction of inflorescence height and petal size on both host species. Vectors may therefore in principle discriminate among hosts infected by different strains and affect their efficiency of transmission. Contrary to assumptions of recent hypotheses about the role of host hybrids in the evolution of parasites, hybrids were not generally more susceptible than parental hosts. It is therefore unlikely that the rate of evolution of the pathogen on the parental species is slowed down by selection for specialization on the hybrids.

Key words

Host manipulation Host specialization Plant-pathogen interactions Silene Ustilago violacea 


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  1. Alexander HM (1989) An experimental field study of anther-smut disease of Silene alba caused by Ustilago violacea: genotypic variation and disease incidence. Evolution 43: 835–847Google Scholar
  2. Alexander HM, Antonovics J (1988) Disease spread and population dynamics of anther smut infection of Silene alba caused by Ustilago violacea. J Ecol 76: 91–104Google Scholar
  3. Alexander HM, Maltby A (1990) Anther-smut infection of Silene alba caused by Ustilago violacea: factors determining fungal reproduction. Oecologia 84: 249–253Google Scholar
  4. Alexander HM, Antonovics J, Kelly AW (1993) Genotypic variation in plant disease resistance—physiological resistance in relation to field disease transmission. J Ecol 81: 325–333Google Scholar
  5. Antonovics J, Alexander HM (1992) Epidemiology of anther-smut infection of Silene alba (=S. latifolia) caused by Ustilago violacea: patterns of spore deposition in experimental populations. Proc R Soc Lond B 250: 157–163Google Scholar
  6. Baker HG (1947) Melandrium album and M. dioicum in the Biological Flora of the British Isles. J Ecol 35: 471Google Scholar
  7. Baker HG (1951) The inheritance of certain characters in crosses between Melandrium dioicum and M. album. Genetica 25: 126–156Google Scholar
  8. Biere A, Antonovics J (1996) Sex-specific costs of resistance to the fungal pathogen Ustilago violacea in Silene alba. Evolution (in press)Google Scholar
  9. Boecklen WJ, Spellenberg R (1990) Structure of herbivore communities in two oak (Quercus spp.) hybrid zones. Oecologia 85: 92–100Google Scholar
  10. Brasier CM (1987) The dynamics of fungal speciation. In: Rayner ADM, Brasier CM, Moore D (eds) Evolutionary biology of the fungi. Cambridge University Press, Cambridge, pp 231–260Google Scholar
  11. Burdon JJ (1987) Diseases and plant population biology. Cambridge University Press, CambridgeGoogle Scholar
  12. Burdon JJ, Jarosz AM (1991) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. I: Patterns of resistance and racial variation in a large host population. Evolution 45: 205–217Google Scholar
  13. Burdon JJ, Brown AHD, Jarosz AM (1990) The spatial scale of genetic interactions in host-pathogen coevolved systems. In: Burdon JJ, Leather SR (eds) Pests pathogens and plant communities. Blackwell, Oxford, pp 233–247Google Scholar
  14. Castle AJ, Day AW (1984) Isolation and identification of α-tocopherol as an inducer of the parasitic phase of Ustilago violacea. Phytopathology 74: 1194–1200Google Scholar
  15. Day AW, Jones JK (1968) The production and characteristics of diploids in Ustilago violacea. Gen Res 11: 63–81Google Scholar
  16. Day AW, Castle AJ, Cummins JE (1981) Regulation of parasitic development of the smut fungus, Ustilago violacea, by extracts from host plants. Bot Gaz 142: 135–146Google Scholar
  17. De Nooij MP, Van Damme JMM (1988) Variation in pathogenicity among and within populations of the fungus Phomopsis subordinaria infecting Plantago lanceolata. Evolution 42: 1166–1171Google Scholar
  18. Dean HL (1959) Variations in style number and other gynoecial structures in Lychnis alba. Science 130: 42–43Google Scholar
  19. Deml G, Oberwinkel F (1982) Studies in Heterobasidiomycetes, part 24. On Ustilago violacea (Pers.) Rouss. from Saponaria officinalis. Phytopathol Z 104: 345–356Google Scholar
  20. Ennos RA, Swales KW (1991) Genetic variation in a fungal pathogen: response to host defensive chemicals. Evolution 45: 190–204Google Scholar
  21. Ericson L, Burdon JJ, Wennström A (1993) Inter-specific host hybrids and phalacrid beetles implicated in the local survival of smut pathogens. Oikos 68: 393–400Google Scholar
  22. Floate KD, Whitham TG (1993) The “hybrid bridge” hypothesis: host shifting via plant hybrid swarms. Am Nat 141: 651–662Google Scholar
  23. Fritz RS, Nichols-Orians CM, Brunsfeld SJ (1994) Interspecific hybridization of plants and resistance to herbivores: hypotheses, genetics, and variable responses in a diverse herbivore community. Oecologia 97: 106–117Google Scholar
  24. Garber ED, Baird ML, Chapman DJ (1975) Genetics of Ustilago violacea. I. Carotenoid mutants and carotenogenesis. Bot Gaz 136: 341–346Google Scholar
  25. Garber ED, Baird ML, Weiss LM (1978) Genetics of Ustilago violacea. II. Polymorphism of color and nutritional requirements of sporidia from natural populations. Bot Gaz 139: 261–265Google Scholar
  26. Goldschmidt V (1928) Vererbungsversuche mit den biologischen Arten des Antherenbrandes (Ustilago violacea Pers.). Ein Beitrag zur Frage der parasitären Spezialisierung. Z Bot 21: 1–90Google Scholar
  27. Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21: 243–273Google Scholar
  28. Jarosz AM, Burdon JJ (1991) Host-pathogen interactions in natural populations of Linum marginale and Melampsora lini. II. Local and regional variation in patterns of resistance and racial structure. Evolution 45: 1618–1627Google Scholar
  29. Jennersten O (1988) Insect dispersal of fungal disease: effects of Ustilago infection on pollinator attraction in Viscaria vulgaris. Oikos 51: 163–170Google Scholar
  30. Jennersten O, Kwak MM (1991) Competition for bumblebee visitation between Melampyrum pratense and Viscaria vulgaris with healthy and Ustilago infected flowers. Oecologia 86: 88–98Google Scholar
  31. Johnson SG, Delph LF, Elderkin CL (1995) The effect of petal-size manipulation on pollen removal, seed set, and insect-visitor behavior in Campanula americana. Oecologia 102: 174–179Google Scholar
  32. Kay QON, Lack AJ, Bamber FC, Davies CR (1984) Differences between sexes in floral morphology, nectar production and insect visits in a dioecious species, Silene dioica. New Phytol 98: 515–529Google Scholar
  33. Klinkhamer PGL, De Jong TJ, De Bruin G (1989) Plant size and pollinator visitation in Cynoglossum officinale. Oikos 54: 201–204Google Scholar
  34. Klinkhamer PGL, De Jong TJ, Metz JAJ (1994) Why plants can be too attractive—a discussion of measures to estimate male fitness. J Ecol 82: 191–194Google Scholar
  35. Lawrence GJ, Burdon JJ (1989) Flax rust from Linum marginale: variation in a natural host-pathogen interaction. Can J Bot 67: 3192–3198Google Scholar
  36. Lee JA (1981) Variation in the infection of Silene dioica (L.) Clairv. by Ustilago violacea (Pers.) Fuckel in north west England. New Phytol 87: 81–89Google Scholar
  37. Liro JI (1924) Die Ustilagineen Finnlands, vol I. Helsinki. Annales Academicae Scienti Fennicae Serie A, HelsinkiGoogle Scholar
  38. Marden J (1984) Remote perception of flower nectar by bumblebees. Oecologia 64: 232–240Google Scholar
  39. Norusis MJ (1986) SPSS-PC+: statistical package for the social sciences. SPSS, ChicagoGoogle Scholar
  40. Parker MA (1985) Local population differentiation for compatibility in an annual legume and its host-specific fungal pathogen. Evolution 39: 713–723Google Scholar
  41. Parker MA (1992) Constraints on the evolution of resistance to pests and pathogens. In: Ayres PG (ed) Pests and pathogens. Plant responses to foliar attack. BIOS, Oxford, pp 181–197Google Scholar
  42. Rausher MD (1984) Tradeoffs in performance on different hosts: evidence from within- and between-site variation in the beetle Deloyala guttata. Evolution 38: 582–595Google Scholar
  43. Real LA, Marschall EA, Roche BM (1992) Individual behaviour and pollination ecology: implications for the spread of sexually transmitted diseases. In: DeAngelis DL, Gross LJ (eds) Individual-based models and approaches in ecology. Chapman and Hall, New York, pp 492–508Google Scholar
  44. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223–225Google Scholar
  45. Roy BA (1994) The use and abuse of pollinators by fungi. Trends Ecol Evol 9: 335–339Google Scholar
  46. Ruddat M, Kokontis JM (1988) Host-parasite recognition in Ustilago violacea—Silene alba. In: Chapman GP, Ainsworth CC, Chatham CJ (eds) Eukaryote cell recognition. Cambridge University Press, Cambridge, pp 275–292Google Scholar
  47. Sage RD, Heyneman D, Lim K, Wilson AC (1986) Wormy mice in a hybrid zone. Nature 324: 60–63Google Scholar
  48. Schmid-Hempel P, Speiser B (1988) Effects of inflorescence size on pollination in Epilobium angustifolium. Oikos 53: 98–104Google Scholar
  49. Shykoff JA, Bucheli E (1995) Pollinator visitation patterns, floral rewards and the probability of transmission of Microbotryum violaceum, a venereal disease of plants. J Ecol 83: 189–198Google Scholar
  50. Sokal RR, Rohlf FJ (1981) Biometry. Freeman, San FranciscoGoogle Scholar
  51. Thompson JN (1994) The coevolutionary process. University of Chicago Press, ChicagoGoogle Scholar
  52. Thrall PH, Jarosz AM (1994) Host-pathogen dynamics in experimental populations of Silene alba and Ustilago violacea. I. Ecological and genetic determinants of disease spread. J Ecol 82: 549–559Google Scholar
  53. Waddington KD (1981) Factors influencing pollen flow in bumblebee-pollinated Delphinium virescens. Oikos 37: 153–159Google Scholar
  54. Whitham TG (1989) Plant hybrid zones as sinks for pests. Science 244: 1490–1493Google Scholar
  55. Zillig H (1921) Ueber spezialisierte Formen beim Antherenbrand, Ustilago violacea (Pers.). Fuck Zentralbl Bakteriol 53: 33–74Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Arjen Biere
    • 1
  • Sonja Honders
    • 1
  1. 1.Department of Plant Population BiologyNetherlands Institute of Ecology, NIOO-CTOHeterenThe Netherlands

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