Advertisement

Viral pathogens and the advantage of sex in the perennial grass Anthoxanthum odoratum

  • Steven E. Kelley

Summary

The ubiquity of sexual reproduction among plants and animals remains one of the major unresolved paradoxes of modern evolutionary biology. In order for sex to be maintained in populations, sex must confer immediate and substantial fitness benefits. Theoreticians have proposed numerous mechanisms to explain how such advantages arise, but experimental data are few. In one well-studied population of the perennial grass Anthoxanthum odoratum in a mown North Carolina field, sexual offspring have been found to have significantly higher fitness than asexual offspring. More recent field experiments show that an aphid-transmitted virus, barley yellow dwarf (BYDV)-strain SGV, specifically transmitted by Schizaphus graminum, frequently infects Anthoxanthum progeny soon after transplantation into the field, BYDV infection is asymptomatic in Anthoxanthum, but BYDV-inoculated clones planted directly in the field had significantly lower fitness than healthy controls.

Sexual females have been hypothesized to gain a fitness advantage for their offspring in the presence of pathogens either by providing ‘an escape in time’ from pathogens preadapted to the parental genotype or through the production of rare genotypes, which escape frequency-dependent infection. When parental clones and seed-derived sexual offspring were planted in identical but separate arrays in sites near where the parent was collected, parental clones were twice as frequently infected as sexual offspring. Factors other than genetic variation may have contributed to differences in levels of infection between sexual and asexual progeny: in this experiment, clonally derived asexual offspring tillers were slightly larger than seed-derived sexual tillers; in field experiments, larger plants were more frequently infected than smaller plants. When different families were planted into a common site, there was evidence that genotypes were less frequently infected when locally rare than when common.

Taken together, the data suggest that BYDV infection generates advantages for rare or sexually produced genotypes in Anthoxanthum. The pattern of infection is likely to result from a complex interaction between vector, host, and viral genetics and population structure, vector behaviour, and host and vector dispersal patterns. Sexually produced genotypes appear to benefit because they are both novel and rare, but the observed minority advantage was weak. Other viral, bacterial, and fungal pathogens in this Anthoxanthum population may act as frequency-dependent selective forces in different places in the field, collectively generating the substantial and observed overall fitness advantage of rare genotypes. Further study is needed to elucidate their role. Nevertheless, the data do show that viral pathogens, which are often asymptomatic, play a significant evolutionary role in plant populations.

Keywords

Sexual Reproduction Sexual Offspring Parental Clone Barley Stripe Mosaic Virus Home Site 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Antonovics, J. & Ellstrand, N.C. 1984 Experimental studies of the evolutionary significance of sexual reproduction. I. A test of the frequency—dependent selection hypothesis. Evolution 38, 103–115.CrossRefGoogle Scholar
  2. Barnett, O.W. & Gibson, P.B. 1975 Identification and prevalence of white clover viruses and the resistance of Trifolium species to these viruses. Crop Sci. 15, 32–37.CrossRefGoogle Scholar
  3. Bell, G. 1982 The masterpiece of nature: the evolution and genetics of sexuality. Berkeley: University of California Press.Google Scholar
  4. Bierzychudek, P. 1987 Resolving the paradox of sexual reproduction: a review of experimental tests. In Evolution of sex and its consequences (ed. S. C. Stearns), pp. 163–174. Basel: Birkhauser.Google Scholar
  5. Blua, M.J., Perring, T.M. & Madore, M.A. 1994 Plant virus-induced changes in aphid population development and temporal fluctuations in plant nutrients. J. Chem. Ecol. 20, 691–707.CrossRefGoogle Scholar
  6. Bremermann, H.J. 1980 Sex and polymorphism as strategies in host-pathogen interactions. J. theor. Biol. 87, 671–702.PubMedCrossRefGoogle Scholar
  7. Chiko, A. 1984 Increased virulence of barley stripe mosaic virus for wild oats: evidence of strain selection by host passage. Phytopathology 74, 595–599.CrossRefGoogle Scholar
  8. Cooper, J.I. & MacCallum, F.O. 1984 Viruses and the environment. London; Chapman & Hall.Google Scholar
  9. Dawson, J.R.O. 1967 The adaptation of tomato mosaic virus to resistant tomato plants. Ann. appl. Biol. 60, 209–214.CrossRefGoogle Scholar
  10. Ellstrand, J. & Antonovics, J. 1985 Experimental studies of the evolutionary significance of sexual reproduction. II. A test of the density dependent selection hypothesis. Evolution 39, 657–666.CrossRefGoogle Scholar
  11. Gibbs, A. J. 1980 A plant virus that partially protects its wild legume host against herbivores. Intervirology 13, 42–47.PubMedCrossRefGoogle Scholar
  12. Goodman, R.N., Kiraly, Z. & Wood, K.R. 1986 The biochemistry and physiology of plant disease. Columbia: University of Missouri Press.Google Scholar
  13. Hajimorad, M.R., Kurath, G., Randies, J.W. & Francki, R.I.B. 1991 Change in phenotype and encapsidated RNA segments of an isolate of alfalfa mosaic virus: an influence of host passage. J. gen. Virol. 72, 2885–2893.PubMedCrossRefGoogle Scholar
  14. Hamilton, W.D. 1980 Sex versus non-sex versus parasite. Oikos 35, 282–290.CrossRefGoogle Scholar
  15. Hamilton, W.D. 1990 Sexual reproduction as an adaptation to resist parasites (a review). Proc. natn. Acad. Sci. U.S.A. 87, 3566–3573.CrossRefGoogle Scholar
  16. Hammond, J. 1981 Viruses occurring in Plantago lanceolata in England. Pl. Path. 30, 237–243.CrossRefGoogle Scholar
  17. Holland, J., Spindler, K., Horodyski, F., Grabau, E., Nichol, S. & VandePol, S. 1982 Rapid evolution of RNA genomes. Science, Wash. 215, 1577–1585.CrossRefGoogle Scholar
  18. Hutson, V. & Law, R. 1981 Evolution of recombination in populations experiencing frequency-dependent selection with time delay. Proc. R. Soc. Lond. B 213, 345–359.CrossRefGoogle Scholar
  19. Jaenike, J. 1978 An hypothesis to account for the maintenance of sex within populations. Evol. Theor. 3, 191–194.Google Scholar
  20. Kelley, S.E. 1989a Experimental studies of the evolutionary significance of sexual reproduction. V. A field test of the sib competition lottery hypothesis. Evolution 43, 1054–1065.CrossRefGoogle Scholar
  21. Kelley, S.E. 1989b Experimental studies of the evolutionary significance of sexual reproduction. VI. A glasshouse test of the sib competition hypotheses. Evolution 43, 1066–1074.CrossRefGoogle Scholar
  22. Kelley, S.E. 1993 Viruses and the advantage of sex in Anthoxanthum odoratum: a review. PL Sp. Biol. 8, 217–223.CrossRefGoogle Scholar
  23. Kelley, S.E., Antonovics, J. & Schmitt, J. 1988 A test of the short-term advantage of sexual reproduction. Nature, Lond. 331, 714–716.CrossRefGoogle Scholar
  24. Kennedy, J.S., Day, M.F. & Eastop, V.F. 1962 A conspectus of aphids as vectors of plant viruses. London: Commonwealth Institute of Entomology.Google Scholar
  25. Kirkley, A.F. 1993 The adaptive significance of progeny dispersal in relation to viral disease. (M.S. thesis, Washington State University, Pullman.)Google Scholar
  26. Kondrashov, A.S. 1984 Deleterious mutations as an evolutionary factor. 1. The advantage of recombination. Genet. Res. 44, 199–217.PubMedCrossRefGoogle Scholar
  27. Kondrashov, A.S. 1988 Deleterious mutations and the evolution of sexual reproduction. Nature, Lond. 336, 435–440.CrossRefGoogle Scholar
  28. Kurstak, E. (ed.) 1981 Handbook of plant virus infections. New York: Elsevier.Google Scholar
  29. Lively, C.M. 1987 Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature, Lond. 328, 519–521.CrossRefGoogle Scholar
  30. Lively, CM., Craddock, C & Vrijenhoek, R.C 1990 Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature, Lond. 344, 864–866.CrossRefGoogle Scholar
  31. MacClement, W.D. & Richards, M.G. 1956 Viruses in wild plants. Can. J. Bot. 34, 793–799.CrossRefGoogle Scholar
  32. MacKenzie, S. 1985 Reciprocal transplantation to study local specialisation and the measurement of components of fitness. Ph.D. thesis, University College of North Wales, Bangor.Google Scholar
  33. Maynard Smith, J. 1978 The evolution of sex. Cambridge University Press.Google Scholar
  34. Michod, R.E. & Levin, B.R. 1988 The evolution of sex: an examination of current ideas. Sunderland, Massachusetts: Sinauer Associates.Google Scholar
  35. Power, A.G. 1991 Virus spread and vector dynamics in genetically diverse plant populations. Ecology 72, 233–241.CrossRefGoogle Scholar
  36. Rice, W.R. 1983 Parent-offspring pathogen transmission: a selective agent promoting sexual reproduction. Am. Nat. 121, 187–203.CrossRefGoogle Scholar
  37. Rochow, W.F., Hu, J.S., Forster, R.L. & Hsu, H.T. 1987 Pl. Dis. 71, 272–275.CrossRefGoogle Scholar
  38. Rochow, W.F. & Duffus, J.E. 1981 Luteoviruses and yellows diseases. In Handbook of plant infections and comparative diagnosis (ed. E. Kurstak), pp. 147–170. Amsterdam: Elsevier.Google Scholar
  39. Schmitt, J. & Antonovics, J. 1986 Experimental studies of the evolutionary significance of sexual reproduction. IV. Effects of neighbor relatedness and aphid infestation on seedling performance. Evolution 40, 837–842.CrossRefGoogle Scholar
  40. Shepherd, RJ., Richins, R.D., Duffus, J.I. & Handley, M.K. 1987 Figwort mosaic virus: properties of the virus and its adaptation to a new host. Phytopathology 77, 1668–1673.CrossRefGoogle Scholar
  41. Steinhauer, D.A. & Holland, J.J. 1987 Rapid evolution of RNA viruses. A. Rev. Microbiol. 41, 409–433.CrossRefGoogle Scholar
  42. Tooby, J. 1982 Pathogens, polymorphism, and the evolution of sex. J. theor. Biol. 97, 557–576.PubMedCrossRefGoogle Scholar
  43. Williams, G.C 1975 Sex and evolution. Princeton, New Jersey: Princeton University Press.Google Scholar
  44. Yahara, T. & Oyama, K. 1993 Effects of virus infection on demographic traits of an agamospermous population of Eupatorium chínense (Astevaceae). Oecología 96, 310–315.CrossRefGoogle Scholar
  45. Yarwood, CE. 1979 Host passage effects with plant viruses. Adv. Virus Res. 25, 169–190.PubMedCrossRefGoogle Scholar
  46. Zimmern, D. 1988 RNA viruses. In RNA genetics, vol. 2 (ed. E. Domingo, J. J. Holland & P. Ahlquist), pp. 211–240. Boca Raton, Florida: CRC Press.Google Scholar

Copyright information

© The Royal Society 1997

Authors and Affiliations

  • Steven E. Kelley
    • 1
  1. 1.Department of BiologyEmory UniversityAtlantaUSA

Personalised recommendations