AN EMPIRICAL STUDY OF THE EVOLUTION OF VIRULENCE UNDER BOTH HORIZONTAL AND VERTICAL TRANSMISSION

Abstract According to current thinking, a parasite's transmission mode will be a major determinant of virulence, defined as the harm induced by parasites to their hosts. With horizontal transmission, virulence will increase as a byproduct of a trade‐off between fitness gained through increased among‐host transmission(infectivity) and fitness lost through increased virulence. With vertical transmission, virulence will decrease because a parasite's reproductive potential will be maximized only by decreasing harm to te host, allowing parasite transmission to more host offspring. To test both predictions, we transmitted barley stripe mosaic virus (BSMV) horizontally and then vertically in its host, barley (Hordeum vulgare). After four genrations of horizontal transmission, we observed a nearly two fold increase in horizontal infectivity and nearly tripled virulence. After three generation of subsequent vertical transmission, we observed a modest (16%) increase in vertical transmissibility and a large (40%) reduction in virulence. Increased horizontal transmission is often due to increased pathogen replication which, in turn, causes increased virulence. However, we found no correlation between within‐host virus concentration and virulence, indicating that the observed changes in virulence were not due to changes in viral titer. Finally, horizontally transmitted BSMV had reduced vertical transmission and vertically transmitted BSMV had reduced horizontal infectivity. These two observations suggest that, in nature, in different host populations with varying opportunities for horizontal and vertical transmission, different viral strains may be favored.

[1]  M. Lipsitch,et al.  Virulence and transmission modes of two microsporidia in Daphnia magna , 1995, Parasitology.

[2]  M. Kakehashi Populations and infectious diseases: Dynamics and evolution , 1996, Researches on Population Ecology.

[3]  R. Lenski,et al.  TRADEOFF BETWEEN HORIZONTAL AND VERTICAL MODES OF TRANSMISSION IN BACTERIAL PLASMIDS , 1998, Evolution; international journal of organic evolution.

[4]  N. Yamamura Evolution of mutualistic symbiosis: A differential equation model , 1996, Researches on Population Ecology.

[5]  D. Ebert,et al.  THE INFLUENCE OF HOST DEMOGRAPHY ON THE EVOLUTION OF VIRULENCE OF A MICROSPORIDIAN GUT PARASITE , 1997, Evolution; international journal of organic evolution.

[6]  M A Nowak,et al.  Superinfection and the evolution of parasite virulence. , 1994, Proceedings. Biological sciences.

[7]  Mark Westoby,et al.  PARASITE MEDIATION IN ECOLOGICAL INTERACTIONS , 1986 .

[8]  M. Nowak,et al.  The population dynamics of vertically and horizontally transmitted parasites , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  J. Bull,et al.  SELECTION OF BENEVOLENCE IN A HOST–PARASITE SYSTEM , 1991, Evolution; international journal of organic evolution.

[10]  J. Bull,et al.  Virulence evolution in a virus obeys a trade off , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  K. Clay,et al.  Potential versus actual contribution of vertical transmission to pathogen fitness , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  H. Fraenkel-conrat,et al.  The rod-shaped plant viruses , 1986 .

[13]  A. O. Jackson,et al.  The barley stripe mosaic virus 58-kilodalton beta(b) protein is a multifunctional RNA binding protein , 1997, Journal of virology.

[14]  N. Yamamura Vertical transmission and evolution of mutualism from parasitism , 1993 .

[15]  D. Brooks,et al.  Evolutionary biology of parasites. , 1981, Monographs in population biology.

[16]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[17]  V. Dolja,et al.  Hordeiviruses Structure and Replication , 1986 .

[18]  L. Bolis,et al.  Parasite-Host Associations : Coexistence or Conflict? , 1991 .

[19]  D. Tompkins,et al.  Ectoparasite virulence is linked to mode of transmission , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  J. Koella,et al.  Virulence, parasite mode of transmission, and host fluctuating asymmetry , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[21]  R M May,et al.  Coevolution of hosts and parasites , 1982, Parasitology.

[22]  P. Ewald,et al.  Host-Parasite Relations, Vectors, and the Evolution of Disease Severity , 1983 .

[23]  D. Ebert Virulence and Local Adaptation of a Horizontally Transmitted Parasite , 1994, Science.

[24]  R. Fekety Host-Parasite Relationships and the Pathogenesis of Infectious Diseases , 1982 .

[25]  S. Frank,et al.  Models of plant-pathogen coevolution. , 1992, Trends in genetics : TIG.

[26]  T. W. Carroll,et al.  Seed transmissibility of two strains of barley stripe mosaic virus. , 1972, Virology.

[27]  Robin Cooke,et al.  Foundations of Parasitology , 1986 .

[28]  M. Palomar Concentration and Infectivity of Barley Stripe Mosaic Virus in Barley , 1976 .

[29]  W. Hamilton Sex versus non-sex versus parasite , 1980 .

[30]  K. Clay,et al.  Trade‐off between Virulence and Vertical Transmission and the Maintenance of a Virulent Plant Pathogen , 1998, The American Naturalist.

[31]  Martin A Nowak,et al.  THE EVOLUTION OF VIRULENCE IN PATHOGENS WITH VERTICAL AND HORIZONTAL TRANSMISSION , 1996, Evolution; international journal of organic evolution.

[32]  M. Eigen,et al.  What is a quasispecies? , 2006, Current topics in microbiology and immunology.

[33]  A. O. Jackson,et al.  Hordeivirus isolation and RNA extraction. , 1998, Methods in molecular biology.

[34]  B. J. Winer Statistical Principles in Experimental Design , 1992 .

[35]  Robert L. Mason,et al.  Statistical Principles in Experimental Design , 2003 .

[36]  R. Copeland Assaying levels of plant virus by ELISA. , 1998, Methods in molecular biology.

[37]  G. Foster,et al.  Plant virology protocols : from virus isolation to transgenic resistance , 1998 .

[38]  P. Ewald Transmission Modes and Evolution of the Parasitism‐Mutualism Continuum a , 1987, Annals of the New York Academy of Sciences.

[39]  R. W. Jones,et al.  Identification of barley stripe mosaic virus genes involved in viral RNA replication and systemic movement. , 1990, The EMBO journal.

[40]  Martin A. Nowak,et al.  Superinfection and the evolution of parasite virulence , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[41]  R. Timian The range of symbiosis of barley and barley stripe mosaic virus. , 1974 .

[42]  E. Herre Population Structure and the Evolution of Virulence in Nematode Parasites of Fig Wasps , 1993, Science.

[43]  A. O. Jackson,et al.  The barley stripe mosaic virus gamma b gene encodes a multifunctional cysteine-rich protein that affects pathogenesis. , 1994, The Plant cell.

[44]  H. Mckinney,et al.  Biological Characteristics of Barley Stripe-Mosaic Virus Strains and Their Evolution , 1965 .