Spatial structure mitigates fitness costs in host-parasite coevolution

American Naturalist

Volumn 183, Issue 3, 2014, Pages

  Ashby, Ben ^a   Gupta, Sunetra ^a   Buckling, Angus ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Fitness costs; Host parasite coevolution; Resistance and infectivity range; Spatial structure

Indexed keywords

ANIMAL; ARTICLE; BACTERIOPHAGE; BACTERIUM; BIOLOGICAL MODEL; EVOLUTION; HOST PATHOGEN INTERACTION; PHYSIOLOGY; REPRODUCTIVE FITNESS; VIROLOGY;

ANIMALS; BACTERIA; BACTERIOPHAGES; BIOLOGICAL EVOLUTION; GENETIC FITNESS; HOST-PATHOGEN INTERACTIONS; MODELS, BIOLOGICAL;

EID: 84894296639     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/674826     Document Type: Article

References (73)

1. Agrawal, A. F., and C. M. Lively. 2002. Infection genetics: gene-forgene versus matching-alleles models and all points in between. Evolutionary Ecology Research 4:79-90.
2. Agrawal, A. F., and C. M. Lively. 2003. Modelling infection as a two-step process combining gene-for-gene and matching-allele genetics. Proceedings of the Royal Society B: Biological Sciences 270:323-334.
3. Bak, P., and C. Chao. 1990. A forest-fire model and some thoughts on turbulence. Physics Letters A 147:297-300.
4. Best, A., S. Webb, A. White, and M. Boots. 2011. Host resistance and coevolution in spatially structured populations. Proceedings of the Royal Society B: Biological Sciences 278:2216-2222.
5. Bohannan, B. J. M., B. Kerr, C. M. Jessup, J. B. Hughes, and G. Sandvik. 2002. Trade-offs and coexistence in microbial microcosms. Antonie van Leeuwenhoek 81:107-115.
6. Bohannan, B. J. M., and R. E. Lenski. 2000. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecology Letters 3:362-377.
7. Boots, M., and A. Sasaki. 1999. "Small worlds" and the evolution of virulence: infection occurs locally and at a distance. Proceedings of the Royal Society B: Biological Sciences 266:1933-1938.
8. Brockhurst, M. A., A. Buckling, and P. B. Rainey. 2006. Spatial heterogeneity and the stability of host-parasite coexistence. Journal of Evolutionary Biology 19:374-379.
9. Brockhurst, M. A., A. D. Morgan, P. B. Rainey, and A. Buckling. 2003. Population mixing accelerates coevolution. Ecology Letters 6:975-979.
10. Buckling, A., and P. B. Rainey. 2002a. Antagonistic coevolution between a bacterium and a bacteriophage. Proceedings of the Royal Society B: Biological Sciences 269:931-936.
11. Buckling, A., and P. B. Rainey. 2002b. The role of parasites in sympatric and allopatric host diversification. Nature 420:496-499.
12. Buckling, A., Y. Wei, R. C. Massey, M. A. Brockhurst, and M. E. Hochberg. 2006. Antagonistic coevolution with parasites increases the cost of host deleterious mutations. Proceedings of the Royal Society B: Biological Sciences 273:45-49.
13. Burdon, J. J., and P. H. Thrall. 1999. Spatial and temporal patterns in coevolving plant and pathogen associations. American Naturalist 153(suppl.):S15-S33.
14. Campos, P. R. A., P. S. C. A. Neto, V. M. de Oliveira, and I. Gordo. 2008. Environmental heterogeneity enhances clonal interference. Evolution 62:1390-1399.
15. Carius, H. J., T. J. Little, and D. Ebert. 2001. Genetic variation in a host-parasite association: potential for coevolution and frequencydependent selection. Evolution 55:1136-1145.
16. Chao, L., B. R. Levin, and F. M. Stewart. 1977. A complex community in a simple habitat: an experimental study with bacteria and phage. Ecology 58:369-378.
17. Comins, H. N., M. P. Hassell, and R. M. May. 1992. The spatial dynamics of host-parasitoid systems. Journal of Animal Ecology 61:735-748.
18. Damgaard, C. 1999. Coevolution of a plant host-pathogen gene-forgene system in a metapopulation model without cost of resistance or cost of virulence. Journal of Theoretical Biology 201:1-12.
19. Decaestecker, E., S. Gaba, J. A. M. Raeymaekers, R. Stoks, L. Van Kerckhoven, D. Ebert, and L. De Meester. 2007. Host-parasite "Red Queen" dynamics archived in pond sediment. Nature 450:870-873.
20. Eames, K. T. D., and M. J. Keeling. 2002. Modeling dynamic and network heterogeneities in the spread of sexually transmitted diseases. Proceedings of the National Academy of Sciences of the USA 99:13330-13335.
21. Faruque, S. M., K. Biswas, S. M. N. Udden, Q. S. Ahmad, D. A. Sack, G. B. Nair, and J. J. Mekalanos. 2006. Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proceedings of the National Academy of Sciences of the USA 103:6350-6355.
22. Fenton, A., J. Antonovics, and M. A. Brockhurst. 2009. Inverse-genefor-gene infection genetics and coevolutionary dynamics. American Naturalist 174:E230-E242.
23. Fenton, A., J. Antonovics, and M. A. Brockhurst. 2012. Two-step infection processes can lead to coevolution between functionally independent infection and resistance pathways. Evolution 66:2030-2041.
24. Flor, H. H. 1956. The complementary genetic systems in flax and flax rust. Advances in Genetics 8:29-54.
25. Forde, S. E., R. E. Beardmore, I. Gudelj, S. S. Arkin, J. N. Thompson, and L. D. Hurst. 2008. Understanding the limits to generalizability of experimental evolutionary models. Nature 455:220-223.
26. Forde, S. E., J. N. Thompson, and B. J. M. Bohannan. 2004. Adaptation varies through space and time in a coevolving host-parasitoid interaction. Nature 431:841-844.
27. Forde, S. E., J. N. Thompson, and B. J. M. Bohannan. 2007. Gene flow reverses an adaptive cline in a coevolving host-parasitoid interaction. American Naturalist 169:794-801.
28. Frank, S. A. 1993. Coevolutionary genetics of plants and pathogens. Evolutionary Ecology 7:45-75.
29. Gallet, R., Y. Shao, and I.-N. Wang. 2009. High adsorption rate is detrimental to bacteriophage fitness in a biofilm-like environment. BMC Evolutionary Biology 9:241.
30. Gandon, S., A. Buckling, E. Decaestecker, and T. Day. 2008. Hostparasite coevolution and patterns of adaptation across time and space. Journal of Evolutionary Biology 21:1861-1866.
31. Gandon, S., Y. Capowiez, Y. Dubois, and Y. Michalakis. 1996. Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society B: Biological Sciences 263:1003-1009.
32. Gomez, P., and A. Buckling. 2011. Bacteria-phage antagonistic coevolution in soil. Science 332:106-109.
33. Haerter, J. O., A. Trusina, and K. Sneppen. 2011. Targeted bacterial immunity buffers phage diversity. Journal of Virology 85:10554-10560.
34. Hall, A. R., P. D. Scanlan, A. D. Morgan, and A. Buckling. 2011. Host-parasite coevolutionary arms races give way to fluctuating selection. Ecology Letters 14:635-642.
35. Haraguchi, Y., and A. Sasaki. 2000. The evolution of parasite virulence and transmission rate in a spatially structured population. Journal of Theoretical Biology 203:85-96.
36. Hartvigsen, G., and S. Levin. 1997. Evolution and spatial structure interact to influence plant-herbivore population and community dynamics. Proceedings of the Royal Society B: Biological Sciences 264:1677-1685.
37. Hassell, M. P., R. M. May, S. W. Pacala, and P. L. Chesson. 1991. The persistence of host-parasitoid associations in patchy environments. I. A general criterion. American Naturalist 138:568-583.
38. Heilmann, S., K. Sneppen, and S. Krishna. 2010. Sustainability of virulence in a phage-bacterial ecosystem. Journal of Virology 84: 3016-3022.
39. Heilmann, S., K. Sneppen, and S. Krishna. 2012. Coexistence of phage and bacteria on the boundary of self-organized refuges. Proceedings of the National Academy of Sciences of the USA 109:12828-12833.
40. Hellweger, F. L., and V. Bucci. 2009. A bunch of tiny individuals: individual-based modeling for microbes. Ecological Modelling 220: 8-22.
41. Hochberg, M. E., and M. van Baalen. 1998. Antagonistic coevolution over productivity gradients. American Naturalist 152:620-634.
42. Jansen, V. A. A., and M. van Baalen. 2006. Altruism through beard chromodynamics. Nature 440:663-666.
43. Keeling, M. J., M. E. Woolhouse, D. J. Shaw, L. Matthews, M. Chase-Topping, D. T. Haydon, S. J. Cornell, et al. 2001. Dynamics of the 2001 UK foot and mouth epidemic: stochastic dispersal in a heterogeneous landscape. Science 294:813-817.
44. Kerr, B., C. Neuhauser, B. J. M. Bohannan, and A. M. Dean. 2006. Local migration promotes competitive restraint in a host-pathogen "tragedy of the commons. " Nature 442:75-78.
45. King, K. C., L. F. Delph, J. Jokela, and C. M. Lively. 2009. The geographic mosaic of sex and the Red Queen. Current Biology 19: 1438-1441.
46. Koskella, B., J. N. Thompson, G. M. Preston, and A. Buckling. 2011. Local biotic environment shapes the spatial scale of bacteriophage adaptation to bacteria. American Naturalist 177:440-451.
47. Levin, B. R., and J. J. Bull. 2004. Population and evolutionary dynamics of phage therapy. Nature Reviews Microbiology 2:166-173.
48. Little, T. J., K. Watt, and D. Ebert. 2006. Parasite-host specificity: experimental studies on the basis of parasite adaptation. Evolution 60:31-38.
49. Lively, C. M. 1987. Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature 328:519-521.
50. Lopez-Pascua, L. D. C., and A. Buckling. 2008. Increasing productivity accelerates host-parasite coevolution. Journal of Evolutionary Biology 21:853-860.
51. Lopez-Pascua, L. D. C., S. Gandon, and A. Buckling. 2012. Abiotic heterogeneity drives parasite local adaptation in coevolving bacteria and phages. Journal of Evolutionary Biology 25:187-195.
52. Matz, C., D. McDougald, A. M. Moreno, P. Y. Yung, F. H. Yildiz, and S. Kjelleberg. 2005. Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae. Proceedings of the National Academy of Sciences of the USA 102: 16819-16824.
53. Mitchell, M., M. D. Thomure, and N. L. Williams. 2006. The role of space in the success of coevolutionary learning. Pages 118-124 in Proceedings, Artificial Life X: Tenth International Conference on the Simulation and Synthesis of Living Systems. MIT Press, Cambridge, MA.
54. Mizoguchi, K., M. Morita, C. R. Fischer, M. Yoichi, Y. Tanji, and H. Unno. 2003. Coevolution of bacteriophage PP01 and Escherichia coli O157:H7 in continuous culture. Applied and Environmental Microbiology 69:170-176.
55. Morgan, A. D., M. A. Brockhurst, L. D. C. Lopez-Pascua, C. Pal, and A. Buckling. 2007. Differential impact of simultaneous migration on coevolving hosts and parasites. BMC Evolutionary Biology 7: 1.
56. Morgan, A. D., S. Gandon, and A. Buckling. 2005. The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437:253-256.
57. Pascual, M. 1993. Diffusion-induced chaos in a spatial predator-prey system. Proceedings of the Royal Society B: Biological Sciences 251:1-7.
58. Poullain, V., S. Gandon, M. A. Brockhurst, and A. Buckling. 2008. The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage. Evolution 62:1-11.
59. Rand, D. A., M. Keeling, and H. B. Wilson. 1995. Invasion, stability and evolution to criticality in spatially extended, artificial hostpathogen ecologies. Proceedings of the Royal Society B: Biological Sciences 259:55-63.
60. Read, J. M., and M. J. Keeling. 2003. Disease evolution on networks: the role of contact structure. Proceedings of the Royal Society B: Biological Sciences 270:699-708.
61. Rhodes, C. J., and R. M. Anderson. 1996. Persistence and dynamics in lattice models of epidemic spread. Journal of Theoretical Biology 180:125-133.
62. Sasaki, A. 2000. Host-parasite coevolution in a multilocus gene-forgene system. Proceedings of the Royal Society B: Biological Sciences 267:2183-2188.
63. Scanlan, P. D., A. R. Hall, L. D. C. Lopez-Pascua, and A. Buckling. 2011. Genetic basis of infectivity evolution in a bacteriophage. Molecular Ecology 25:1-9.
64. Schulte, R. D., C. Makus, B. Hasert, N. K. Michiels, and H. Schulenburg. 2010. Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proceedings of the National Academy of Sciences of the USA 107:7359-7364.
65. Shannon, C. E. 1948. A mathematical theory of communication. Bell System Technical Journal 27:379-423.
66. Thompson, J. N. 1994. The coevolutionary process. University of Chicago Press, Chicago.
67. Thompson, J. N., and J. J. Burdon. 1992. Gene-for-gene coevolution between plants and parasites. Nature 360:121-125.
68. Thrall, P. H., and J. J. Burdon. 2002. Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction. Evolution 56:1340-1351.
69. Thrall, P. H., and J. J. Burdon. 2003. Evolution of virulence in a plant host-pathogen metapopulation. Science 299:1735-1737.
70. Vos, M., P. J. Birkett, E. Birch, R. I. Griffiths, and A. Buckling. 2009. Local adaptation of bacteriophages to their bacterial hosts in soil. Science 325:833.
71. Webster, J. P., and M. E. J. Woolhouse. 1999. Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Proceedings of the Royal Society B: Biological Sciences 266:391-396.
72. Weitz, J. S., H. Hartman, and S. A. Levin. 2005. Coevolutionary arms races between bacteria and bacteriophage. Proceedings of the National Academy of Sciences of the USA 102:9535-9540.
73. Zaman, L., S. Devangam, and C. Ofria. 2011. Rapid host-parasite coevolution drives the production and maintenance of diversity in digital organisms. Pages 219-226 in Proceedings of the 13th Annual Conference on Genetic and Evolutionary Computation. ACM, New York.