Host–parasite coevolution: why changing population size matters

Zoology

Volumn 119, Issue 4, 2016, Pages 330-338

  Papkou, Andrei ^a   Gokhale, Chaitanya S ^b   Traulsen, Arne ^c   Schulenburg, Hinrich ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b MASSEY UNIVERSITY   (New Zealand)

^c MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

Author keywords

Genetic drift; Host parasite coevolution; Negative frequency dependent selection; Population bottlenecks; Population size dynamics; Recurrent selective sweeps

Indexed keywords

ADAPTATION; ANIMAL; EVOLUTION; GENE FREQUENCY; GENETICS; HOST PARASITE INTERACTION; PARASITE; POPULATION DYNAMICS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; GENE FREQUENCY; HOST-PARASITE INTERACTIONS; PARASITES; POPULATION DYNAMICS;

EID: 84965008662     PISSN: 09442006     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.zool.2016.02.001     Document Type: Review

References (127)

1. Abel, S., Abel zur Wiesch, P., Chang, H.H., Davis, B.M., Lipsitch, M., Waldor, M.K., Sequence tag-based analysis of microbial population dynamics. Nat. Meth. 12 (2015), 223–226.
2. Agrawal, A., Lively, C.M., Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evol. Ecol. Res. 4 (2002), 79–90.
3. Altizer, S., Harvell, D., Friedle, E., Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol. Evol. 18 (2003), 589–596.
4. Anderson, R.M., May, R.M., Infectious diseases and population cycles of forest insects. Science 210 (1980), 658–661.
5. Anderson, R.M., May, R.M., Infectious Diseases of Humans: Dynamics and Control. 1992, Oxford University Press reprint edition.
6. Anderson, R.M., Grenfell, B.T., May, R.M., Oscillatory fluctuations in the incidence of infectious disease and the impact of vaccination: time series analysis. J. Hyg. Camb. 93 (1984), 587–608.
7. Ashby, B., Gupta, S., Parasitic castration promotes coevolutionary cycling but also imposes a cost on sex. Evolution 68 (2014), 2234–2244.
8. Auld, S.K.J.R., Wilson, P.J., Little, T.J., Rapid change in parasite infection traits over the course of an epidemic in a wild host-parasite population. Oikos 123 (2014), 232–238.
9. Barrett, L.G., Thrall, P.H., Burdon, J.J., Linde, C.C., Life history determines genetic structure and evolutionary potential of host–parasite interactions. Trends Ecol. Evol. 23 (2008), 678–685.
10. Bell, T., Freckleton, R.P., Lewis, O.T., Plant pathogens drive density-dependent seedling mortality in a tropical tree. Ecol. Lett. 9 (2006), 569–574.
11. Ben-Ami, F., Heller, J., Spatial and temporal patterns of parthenogenesis and parasitism in the freshwater snail Melanoides tuberculata. J. Evol. Biol. 18 (2005), 138–146.
12. Bérénos, C., Schmid-Hempel, P., Wegner, K.M., Evolution of host resistance and trade-offs between virulence and transmission potential in an obligately killing parasite. J. Evol. Biol. 22 (2009), 2049–2056.
13. Best, A., White, A., Boots, M., The implications of coevolutionary dynamics to host–parasite interactions. Am. Nat. 173 (2009), 779–791.
14. Best, A., White, A., Kisdi, E., Antonovics, J., Brockhurst, M.A., Boots, M., The evolution of host–parasite range. Am. Nat. 176 (2010), 63–71.
15. Betts, A., Kaltz, O., Hochberg, M.E., Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages. Proc. Natl. Acad. Sci. USA 111 (2014), 11109–11114.
16. Biek, R., Henderson, J.C., Waller, L.A., Rupprecht, C.E., Real, L.A., A high-resolution genetic signature of demographic and spatial expansion in epizootic rabies virus. Proc. Natl. Acad. Sci. USA 104 (2007), 7993–7998.
17. Bjørnstad, O.N., Sait, S.M., Stenseth, N.C., Thompson, D.J., Begon, M., The impact of specialized enemies on the dimensionality of host dynamics. Nature 409 (2001), 1001–1006.
18. Black, A.J., McKane, A.J., Stochastic formulation of ecological models and their applications. Trends Ecol. Evol. 27 (2012), 337–345.
19. Boots, M., White, A., Best, A., Bowers, R., How specificity and epidemiology drive the coevolution of static trait diversity in hosts and parasites. Evolution 68 (2014), 1594–1606.
20. Bose, J., Kloesener, M.H., Schulte, R.D., Multiple-genotype infections and their complex effect on virulence. Zoology 119 (2016), 339–349.
21. Brockmann, D., Human mobility and spatial disease dynamics. Schuster, H.G., (eds.) Reviews of Nonlinear Dynamics and Complexity., vol. 2, 2009, Wiley-VCH Verlag, Weinheim, 1–24.
22. Bruning, K., Lingeman, R., Ringelberg, J., Estimating the impact of fungal parasites on phytoplankton populations. Limnol. Oceanogr. 37 (1992), 252–260.
23. Buckling, A., Rainey, P.B., Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. B 269 (2002), 931–936.
24. Chao, L., Fitness of RNA virus decreased by Muller's ratchet. Nature 348 (1990), 454–455.
25. Cheng, T.L., Rovito, S.M., Wake, D.B., Vredenburg, V.T., Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proc. Natl. Acad. Sci. USA 108 (2011), 9502–9507.
26. Coltman, D.W., Pilkington, J.G., Smith, J.A., Pemberton, J.M., Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53 (1999), 1259–1267.
27. Criscione, C.D., Blouin, M.S., Effective sizes of macroparasite populations: a conceptual model. Trends Parasitol. 21 (2005), 212–217.
28. Croze, M., Živković, D., Stephan, W., Hutter, S., Balancing selection on immunity genes: review of the current literature and new analysis in Drosophila melanogaster. Zoology 119 (2016), 322–329.
29. Day, T., Gandon, S., Applying population-genetic models in theoretical evolutionary epidemiology. Ecol. Lett. 10 (2007), 876–888.
30. Decaestecker, E., Gaba, S., Raeymaekers, J.A.M., Stoks, R., Van Kerckhoven, L., Ebert, D., De Meester, L., Host–parasite “Red Queen” dynamics archived in pond sediment. Nature 450 (2007), 870–873.
31. Dieckmann, U., Adaptive dynamics of pathogen–host interactions. Adaptive Dynamics of Infectious Diseases: In Pursuit of Virulence Management, 2002, Cambridge University Press, Cambridge, 39–59.
32. Dieckmann, U., Law, R., The dynamical theory of coevolution: a derivation from stochastic ecological processes. J. Math. Biol. 34 (1996), 579–612.
33. Dobson, A.P., Hudson, P.J., Regulation and stability of a free-living host–parasite system: Trichostrongylus tenuis in red grouse. II. Population models. J. Anim. Ecol. 61 (1992), 487–498.
34. Dobson, A.P., Hudson, P.J., Microparasites: observed patterns in wild animal populations. Grenfell, B.T., Dobson, A.P., (eds.) Ecology of Infectious Diseases in Natural Populations, 1995, Cambridge University Press, Cambridge, 52–89.
35. Donk, E.V., Ringelberg, J., The effect of fungal parasitism on the succession of diatoms in Lake Maarsseveen I (The Netherlands). Freshw. Biol. 13 (1983), 241–251.
36. Duncan, A.B., Little, T.J., Parasite-driven genetic change in a natural population of Daphnia. Evolution 61 (2007), 796–803.
37. Dybdahl, M.F., Lively, C.M., The geography of coevolution: comparative population structures for a snail and its trematode parasite. Evolution 50 (1996), 2264–2275.
38. Ebert, D., Lipsitch, M., Mangin, K.L., The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. Am. Nat. 156 (2000), 459–477.
39. Escarmís, C., Dávila, M., Charpentier, N., Bracho, A., Moya, A., Domingo, E., Genetic lesions associated with Muller's ratchet in an RNA virus. J. Mol. Biol. 264 (1996), 255–267.
40. Ewens, W.J., The probability of survival of a new mutant in a fluctuating environment. Heredity 22 (1967), 438–443.
41. Fenner, F., Fantini, B., Biological Control of Vertebrate Pests: The History of Myxomatosis – an Experiment in Evolution. first edition, 1999, CABI, New York.
42. Frank, S.A., Ecological and genetic models of host–pathogen coevolution. Heredity 67 (1991), 73–83.
43. Frank, S.A., Coevolutionary genetics of plants and pathogens. Evol. Ecol. 7 (1993), 45–75.
44. Gandon, S., Day, T., Evolutionary epidemiology and the dynamics of adaptation. Evolution 63 (2009), 826–838.
45. Gandon, S., Michalakis, Y., Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. J. Evol. Biol. 15 (2002), 45–462.
46. Gandon, S., Capowiez, Y., Dubois, Y., Michalakis, Y., Olivieri, I., Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc. R. Soc. B 263 (1996), 1003–1009.
47. Gandon, S., Agnew, P., Michalakis, Y., Coevolution between parasite virulence and host life-history traits. Am. Nat. 160 (2002), 374–388.
48. Gokhale, C.S., Papkou, A., Traulsen, A., Schulenburg, H., Lotka-Volterra dynamics kills the Red Queen: population size fluctuations and associated stochasticity dramatically change host-parasite coevolution. BMC Evol. Biol., 13, 2013, 254.
49. Gómez, P., Ashby, B., Buckling, A., Population mixing promotes arms race host–parasite coevolution. Proc. R. Soc. B, 282, 2015, 20142297.
50. Gomulkiewicz, R., Holt, R.D., When does evolution by natural selection prevent extinction?. Evolution 49 (1995), 201–207.
51. Gomulkiewicz, R., Thompson, J.N., Holt, R.D., Nuismer, S.L., Hochberg, M.E., Hot spots, cold spots, and the geographic mosaic theory of coevolution. Am. Nat. 156 (2000), 156–174.
52. González-Tortuero, E., Rusek, J., Turko, P., Petrusek, A., Maayan, I., Piálek, L., Tellenbach, C., Gießler, S., Spaak, P., Wolinska, J., Daphnia parasite dynamics across multiple Caullerya epidemics indicate selection against common parasite genotypes. Zoology 119 (2016), 314–321.
53. Greeff, M., Schmid-Hempel, P., Influence of co-evolution with a parasite, Nosema whitei, and population size on recombination rates and fitness in the red flour beetle, Tribolium castaneum. Genetica 138 (2010), 737–744.
54. Gsell, A.S., de Senerpont Domis, L.N., Verhoeven, K.J.F., van Donk, E., Ibelings, B.W., Chytrid epidemics may increase genetic diversity of a diatom spring-bloom. ISME J. 7 (2013), 2057–2059.
55. Hamilton, W.D., Axelrod, R., Tanese, R., Sexual reproduction as an adaptation to resist parasites (a review). Proc. Natl. Acad. Sci. USA 87 (1990), 3566–3573.
56. Härkönen, T., Dietz, R., Reijnders, P., Teilmann, J., Harding, K., Hall, A., Brasseur, S., Siebert, U., Goodman, S.J., Jepson, P.D., The 1988 and 2002 phocine distemper virus epidemics in European harbour seals. Dis. Aquat. Organ. 68 (2006), 115–130.
57. Hayward, A.D., Garnier, R., Watt, K.A., Pilkington, J.G., Grenfell, B.T., Matthews, J.B., Pemberton, J.M., Nussey, D.H., Graham, A.L., Heritable, heterogeneous, and costly resistance of sheep against nematodes and potential feedbacks to epidemiological dynamics. Am. Nat. 184 (2014), S58–S76.
58. Heesterbeek, J.A.P., Roberts, M.G., Mathematical models for microparasites of wildlife. Grenfell, B.T., Dobson, A.P., (eds.) Ecology of Infectious Diseases in Natural Populations, 1995, Cambridge University Press, Cambridge, 90–122.
59. Hesse, E., Buckling, A., Host population bottlenecks drive parasite extinction during antagonistic coevolution. Evolution 70 (2016), 235–240.
60. Ho, S.Y.W., Shapiro, B., Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol. Ecol. Resour. 11 (2011), 423–434.
61. Hochachka, W.M., Dhondt, A.A., Density-dependent decline of host abundance resulting from a new infectious disease. Proc. Natl. Acad. Sci. USA 97 (2000), 5303–5306.
62. Hochberg, M.E., Baalen, M.v., Antagonistic coevolution over productivity gradients. Am. Nat. 152 (1998), 620–634.
63. Hochberg, M.E., Møller, A.P., Insularity and adaptation in coupled victim–enemy associations. J. Evol. Biol. 14 (2001), 539–551.
64. Hoffman, J.I., Simpson, F., David, P., Rijks, J.M., Kuiken, T., Thorne, M.A.S., Lacy, R.C., Dasmahapatra, K.K., High-throughput sequencing reveals inbreeding depression in a natural population. Proc. Natl. Acad. Sci. USA 111 (2014), 3775–3780.
65. Holfeld, H., Fungal infections of the phytoplankton: seasonality, minimal host density, and specificity in a mesotrophic lake. New Phytol. 138 (1998), 507–517.
66. Holmes, J.C., Impact of infectious disease agents on the population growth and geographical distribution of animals. Anderson, R.M., May, R.M., (eds.) Population Biology of Infectious Diseases, 1982, Springer-Verlag, Berlin, 37–51.
67. Hudson, P.J., Dobson, A.P., Macroparasites: observed patterns in naturally fluctuating animal populations. Grenfell, B.T., Dobson, A.P., (eds.) Ecology of Infectious Diseases in Natural Populations, 1995, Cambridge University Press, Cambridge, 144–176.
68. Hudson, P.J., Dobson, A.P., Newborn, D., Prevention of population cycles by parasite removal. Science 282 (1998), 2256–2258.
69. Jones, R.M., Nicas, M., Hubbard, A., Sylvester, M.D., Reingold, A., The infectious dose of Francisella tularensis (Tularemia). Appl. Biosaf. 10 (2005), 227–239.
70. Joop, G., Vilcinskas, A., Coevolution of parasitic fungi and insect hosts. Zoology 119 (2016), 350–358.
71. Killick, S.C., Obbard, D.J., West, S.A., Little, T.J., Parasitism and breeding system variation in North American populations of Daphnia pulex. Ecol. Res. 23 (2008), 235–240.
72. Kimura, M., Stochastic processes in population genetics, with special reference to distribution of gene frequencies and probability of gene fixation. Kojima, K., (eds.) Mathematical Topics in Population Genetics, 1970, Springer-Verlag, Heidelberg, 178–209.
73. Kimura, M., Ohta, T., The average number of generations until fixation of a mutant gene in a finite population. Genetics 61 (1969), 763–771.
74. King, K.C., Delph, L.F., Jokela, J., Lively, C.M., The geographic mosaic of sex and the Red Queen. Curr. Biol. 19 (2009), 1438–1441.
75. Kurze, C., Routtu, J., Moritz, R.F.A., Parasite resistance and tolerance in honeybees at the individual and social level. Zoology 119 (2016), 290–297.
76. Kutzer, M.A.M., Armitage, S.A.O., Maximising fitness in the face of parasites: a review of host tolerance. Zoology 119 (2016), 281–289.
77. Lemey, P., Rambaut, A., Pybus, O.G., HIV evolutionary dynamics within and among hosts. AIDS Rev. 8 (2006), 125–140.
78. Lenski, R.E., May, R.M., The evolution of virulence in parasites and pathogens: reconciliation between two competing hypotheses. J. Theor. Biol. 169 (1994), 253–265.
79. Levin, B.R., Lipsitch, M., Bonhoeffer, S., Population biology, evolution, and infectious disease: convergence and synthesis. Science 283 (1999), 806–809.
80. Lively, C.M., The maintenance of sex: host–parasite coevolution with density-dependent virulence. J. Evol. Biol. 22 (2009), 2086–2093.
81. Lively, C.M., A review of Red Queen models for the persistence of obligate sexual reproduction. J. Hered. 101 (2010), S13–S20.
82. Lively, C.M., Apanius, V., Genetic diversity in host–parasite interactions. Grenfell, B.T., Dobson, A.P., (eds.) Ecology of Infectious Diseases in Natural Populations, 1995, Cambridge University Press, Cambridge, 421–449.
83. Lively, C.M., Jokela, J., Temporal and spatial distributions of parasites and sex in a freshwater snail. Evol. Ecol. Res. 4 (2002), 219–226.
84. Lively, C.M., Johnson, S.G., Delph, L.F., Clay, K., Thinning reduces the effect of rust infection on jewelweed (Impatiens capensis). Ecology 76 (1995), 1859–1862.
85. Lotka, A.J., The growth of mixed populations: two species competing for a common food supply. J. Wash. Acad. Sci. 22 (1932), 461–469.
86. Maldarelli, F., Kearney, M., Palmer, S., Stephens, R., Mican, J., Polis, M.A., Davey, R.T., Kovacs, J., Shao, W., Rock-Kress, D., Metcalf, J.A., Rehm, C., Greer, S.E., Lucey, D.L., Danley, K., Alter, H., Mellors, J.W., Coffin, J.M., HIV populations are large and accumulate high genetic diversity in a nonlinear fashion. J. Virol. 87 (2013), 10313–10323.
87. Marston, M.F., Pierciey, F.J., Shepard, A., Gearin, G., Qi, J., Yandava, C., Schuster, S.C., Henn, M.R., Martiny, J.B.H., Rapid diversification of coevolving marine Synechococcus and a virus. Proc. Natl. Acad. Sci. USA 109 (2012), 4544–4549.
88. May, R.M., Anderson, R.M., Epidemiology and genetics in the coevolution of parasites and hosts. Proc. R. Soc. B 219 (1983), 281–313.
89. McCallum, H., Barlow, N., Hone, J., How should pathogen transmission be modelled?. Trends Ecol. Evol. 16 (2001), 295–300.
90. Middelboe, M., Holmfeldt, K., Riemann, L., Nybroe, O., Haaber, J., Bacteriophages drive strain diversification in a marine Flavobacterium: implications for phage resistance and physiological properties. Environ. Microbiol. 11 (2009), 1971–1982.
91. Milutinović, B., Peuß, R., Ferro, K., Kurtz, J., Immune priming in arthropods: an update focusing on the red flour beetle. Zoology 119 (2016), 254–261.
92. Miyashita, S., Kishino, H., Estimation of the size of genetic bottlenecks in cell-to-cell movement of soil-borne wheat mosaic virus and the possible role of the bottlenecks in speeding up selection of variations in trans-acting genes or elements. J. Virol. 84 (2010), 1828–1837.
93. Morran, L.T., Schmidt, O.G., Gelarden, I.A., Parrish, R.C., Lively, C.M., Running with the Red Queen: host–parasite coevolution selects for biparental sex. Science 333 (2011), 216–218.
94. Otto, S., Whitlock, M., The probability of fixation in populations of changing size. Genetics 146 (1997), 723–733.
95. Parsons, T.L., Quince, C., Plotkin, J.B., Some consequences of demographic stochasticity in population genetics. Genetics 185 (2010), 1345–1354.
96. Patwa, Z., Wahl, L., The fixation probability of beneficial mutations. J. R. Soc. Interface 5 (2008), 1279–1289.
97. Pimentel, D., Population regulation and genetic feedback evolution provides foundation for control of herbivore, parasite, and predator numbers in nature. Science 159 (1968), 1432–1437.
98. Pybus, O.G., Rambaut, A., Evolutionary analysis of the dynamics of viral infectious disease. Nat. Rev. Genet. 10 (2009), 540–550.
99. Quigley, B.J.Z., López, D.G., Buckling, A., McKane, A.J., Brown, S.P., The mode of host–parasite interaction shapes coevolutionary dynamics and the fate of host cooperation. Proc. R. Soc. B 279 (2012), 3742–3748.
100. Råberg, L., Alacid, E., Garces, E., Figueroa, R., The potential for arms race and red queen coevolution in a protist host–parasite system. Ecol. Evol. 4 (2015), 4775–4785.
101. Rambaut, A., Pybus, O.G., Nelson, M.I., Viboud, C., Taubenberger, J.K., Holmes, E.C., The genomic and epidemiological dynamics of human influenza A virus. Nature 453 (2008), 615–619.
102. Redpath, S.M., Mougeot, F., Leckie, F.M., Elston, D.A., Hudson, P.J., Testing the role of parasites in driving the cyclic population dynamics of a gamebird: parasites and population dynamics. Ecol. Lett. 9 (2006), 410–418.
103. Restif, O., Koella, J., Shared control of epidemiological traits in a coevolutionary model of host–parasite interactions. Am. Nat. 161 (2003), 827–836.
104. Roff, D.A., Evolutionary Quantitative Genetics. 1997, Chapman & Hall, New York.
105. Savage, A.E., Sredl, M.J., Zamudio, K.R., Disease dynamics vary spatially and temporally in a North American amphibian. Biol. Conserv. 144 (2011), 1910–1915.
106. Schmid-Hempel, P., Frank, S.A., Pathogenesis, virulence, and infective dose. PLoS Pathog. 3 (2007), 1372–1373.
107. Schulte, R.D., Makus, C., Hasert, B., Michiels, N.K., Schulenburg, H., Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc. Natl. Acad. Sci. USA 107 (2010), 7359–7364.
108. Song, Y., Gokhale, C., Papkou, A., Schulenburg, H., Traulsen, A., Host–parasite coevolution in populations of constant and variable size. BMC Evol. Biol., 15, 2015, 212.
109. Strauß, J.F., Crain, P., Schulenburg, H., Telschow, A., Experimental solution in silico: a custom-designed mathematical model for virulence evolution of Bacillus thuringiensis. Zoology 119 (2016), 359–365.
110. Tee, K.K., Lam, T.T.Y., Chan, Y.F., Bible, J.M., Kamarulzaman, A., Tong, C.Y.W., Takebe, Y., Pybus, O.G., Evolutionary genetics of human enterovirus 71: origin, population dynamics, natural selection, and seasonal periodicity of the VP1 gene. J. Virol. 84 (2010), 3339–3350.
111. Tellier, A., Brown, J.K.M., Stability of genetic polymorphism in host–parasite interactions. Proc. R. Soc. B 274 (2007), 809–817.
112. Tellier, A., Moreno-Gámez, S., Stephan, W., Speed of adaptation and genomic footprints of host–parasite coevolution under arms race and trench warfare dynamics. Evolution 68 (2014), 2211–2224.
113. Thompson, J.N., The Geographic Mosaic of Coevolution. 2005, University of Chicago Press, Chicago.
114. Thrall, P.H., Burdon, J.J., Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal. Plant Pathol. 51 (2002), 169–184.
115. Tompkins, D., Begon, M., Parasites can regulate wildlife populations. Parasitol. Today 15 (1999), 311–313.
116. Utida, S., Cyclic fluctuations of population density intrinsic to the host–parasite system. Ecology 38 (1957), 442–449.
117. van Baalen, M., Coevolution of recovery ability and virulence. Proc. R. Soc. B 265 (1998), 317–325.
118. Velo-Antón, G., Rodríguez, D., Savage, A.E., Parra-Olea, G., Lips, K.R., Zamudio, K.R., Amphibian-killing fungus loses genetic diversity as it spreads across the New World. Biol. Conserv. 146 (2012), 213–218.
119. Vilcinskas, A., The role of epigenetics in host–parasite coevolution: lessons from the model host insects Galleria mellonella and Tribolium castaneum. Zoology 119 (2016), 273–280.
120. Visser, P.B., Brown, D.J.F., Brederode, F.T., Bol, J.F., Nematode transmission of tobacco rattle virus serves as a bottleneck to clear the virus population from defective interfering RNAs. Virology 263 (1999), 155–165.
121. Volterra, V., Variations and fluctuations of the number of individuals in animal species living together. J. Cons. Int. Explor. Mer. 3 (1928), 3–51.
122. Whitlock, M.C., Phillips, P.C., Fowler, K., Persistence of changes in the genetic covariance matrix after a bottleneck. Evolution 56 (2002), 1968–1975.
123. Wildt, D.E., Bush, M., Goodrowe, K.L., Packer, C., Pusey, A.E., Brown, J.L., Joslin, P., O'Brien, S.J., Reproductive and genetic consequences of founding isolated lion populations. Nature 329 (1987), 328–331.
124. Wolinska, J., King, K.C., Environment can alter selection in host–parasite interactions. Trends Parasitol. 25 (2009), 236–244.
125. Woolhouse, M.E.J., Taylor, L.H., Haydon, D.T., Population biology of multihost pathogens. Science 292 (2001), 1109–1112.
126. Woolhouse, M.E.J., Webster, J.P., Domingo, E., Charlesworth, B., Levin, B.R., Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32 (2002), 569–577.
127. Zwart, M.P., Daròs, J.A., Elena, S.F., One is enough: in vivo effective population size is dose-dependent for a plant RNA virus. PLoS Pathog., 7, 2011, e1002122.