Maximising fitness in the face of parasites: a review of host tolerance

Zoology

Volumn 119, Issue 4, 2016, Pages 281-289

  Kutzer, Megan A M ^a   Armitage, Sophie A O ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Ecological immunology; Host fitness; Parasite load; Resistance; Tolerance

Indexed keywords

ANIMAL; ANIMAL PARASITOSIS; BIOLOGICAL MODEL; GENETIC VARIATION; GENETICS; HUMAN; IMMUNOLOGY; REPRODUCTIVE FITNESS;

ANIMALS; GENETIC FITNESS; GENETIC VARIATION; HUMANS; MODELS, IMMUNOLOGICAL; PARASITIC DISEASES, ANIMAL;

EID: 84978386298     PISSN: 09442006     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.zool.2016.05.011     Document Type: Review

References (53)

1. Adelman, J.S., Kirkpatrick, L., Grodio, J.L., Hawley, D.M., House finch populations differ in early inflammatory signaling and pathogen tolerance at the peak of Mycoplasma gallisepticum infection. Am. Nat. 181 (2013), 674–689.
2. Ayres, J.S., Schneider, D.S., A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. PLoS Biol. 6 (2008), 2764–2773.
3. Ayres, J.S., Schneider, D.S., The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biol., 7, 2009, e1000150.
4. Baucom, R.S., de Roode, J.C., Ecological immunology and tolerance in plants and animals. Funct. Ecol. 25 (2011), 18–28.
5. Best, A., White, A., Boots, M., Maintenance of host variation in tolerance to pathogens and parasites. Proc. Natl. Acad. Sci. U.S.A. 105 (2008), 20786–20791.
6. Best, A., White, A., Boots, M., Resistance is futile but tolerance can explain why parasites do not always castrate their hosts. Evolution 64 (2010), 348–357.
7. Best, A., White, A., Boots, M., The coevolutionary implications of host tolerance. Evolution 68 (2014), 1426–1435.
8. Blanchet, S., Rey, O., Loot, G., Evidence for host variation in parasite tolerance in a wild fish population. Evol. Ecol. 24 (2010), 1129–1139.
9. Choisy, M., de Roode, J.C., Mixed infections and the evolution of virulence: effects of resource competition, parasite plasticity, and impaired host immunity. Am. Nat. 175 (2010), E105–E118.
10. Corby-Harris, V., Habel, K.E., Ali, F.G., Promislow, D.E.L., Alternative measures of response to Pseudomonas aeruginosa infection in Drosophila melanogaster. J. Evol. Biol. 20 (2007), 526–533.
11. De Roode, J.C., Lefèvre, T., Behavioral immunity in insects. Insects 3 (2012), 789–820.
12. De Roode, J., Pedersen, A., Hunter, M., Altizer, S., Host plant species affects virulence in monarch butterfly parasites. J. Anim. Ecol. 77 (2008), 120–126.
13. Doeschl-Wilson, A.B., Bishop, S.C., Kyriazakis, I., Villanueva, B., Novel methods for quantifying individual host response to infectious pathogens for genetic analyses. Front. Genet. 3 (2012), 1–9.
14. Feis, M.E., Goedknegt, M.A., Thieltges, D.W., Buschbaum, C., Wegner, K.M., Biological invasions and host–parasite coevolution: different coevolutionary trajectories along separate parasite invasion fronts. Zoology 119 (2016), 366–374.
15. Ferreira, A., Marguti, I., Bechmann, I., Jeney, V., Chora, A., Palha, N.R., Rebelo, S., Henri, A., Beuzard, Y., Soares, M.P., Sickle hemoglobin confers tolerance to Plasmodium infection. Cell 145 (2011), 398–409.
16. Graham, A.L., Shuker, D.M., Pollitt, L.C., Auld, S.K.J.R., Wilson, A.J., Little, T.J., Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Funct. Ecol. 25 (2011), 5–17.
17. Gozzelino, R., Andrade, B.B., Larsen, R., Luz, N.F., Vanoaica, L., Seixas, E., Coutinho, A., Cardoso, S., Rebelo, S., Poli, M., Barral-Netto, M., Darshan, D., Kühn, L.C., Soares, M.P., Metabolic adaptation to tissue iron overload confers tolerance to malaria. Cell Host Microbe 12 (2012), 693–704.
18. Hayward, A.D., Nussey, D.H., Wilson, A.J., Berenos, C., Pilkington, J.G., Watt, K.A., Pemberton, J.M., Graham, A.L., Natural selection on individual variation in tolerance of gastrointestinal nematode infection. PLoS Biol. 12 (2014), 1–13.
19. Hoeksema, J.D., Forde, S.E., A meta-analysis of factors affecting local adaptation between interacting species. Am. Nat. 171 (2008), 275–290.
20. Howick, V.M., Lazzaro, B.P., Genotype and diet shape resistance and tolerance across distinct phases of bacterial infection. BMC Evol. Biol., 14, 2014, 56.
21. Jackson, J.A., Hall, A.J., Friberg, I.M., Ralli, C., Lowe, A., Zawadzka, M., Turner, A.K., Stewart, A., Birtles, R.J., Paterson, S., Bradley, J.E., Begon, M., An immunological marker of tolerance to infection in wild rodents. PLoS Biol. 12 (2014), 1–13.
22. Jamieson, A.M., Pasman, L., Yu, S., Gamradt, P., Homer, R.J., Decker, T., Medzhitov, R., Role of tissue protection in lethal respiratory viral–bacterial coinfection. Science 340 (2013), 1230–1234.
23. Kaltz, O., Shykoff, J.A., Local adaptation in host–parasite systems. Heredity 81 (1998), 361–370.
24. Kause, A., Genetic analysis of tolerance to infections using random regressions: a simulation study. Genet. Res. 93 (2011), 291–302.
25. Kause, A., Ødegård, J., The genetic analysis of tolerance to infections: a review. Front. Genet. 3 (2012), 1–9.
26. Keebaugh, E.S., Schlenke, T.A., Insights from natural host–parasite interactions: the Drosophila model. Dev. Comp. Immunol. 42 (2014), 111–123.
27. Kutzer, M.A.M., Armitage, S.A.O., The effect of diet and time after bacterial infection on fecundity, resistance, and tolerance in Drosophila melanogaster. Ecol. Evol., 6, 2016, 10.1002/ece3.2185.
28. Lefèvre, T., Williams, A.J., de Roode, J.C., Genetic variation in resistance, but not tolerance, to a protozoan parasite in the monarch butterfly. Proc. R. Soc. B 278 (2011), 751–759.
29. Little, T.J., Shuker, D.M., Colegrave, N., Day, T., Graham, A.L., The coevolution of virulence: tolerance in perspective. PLoS Pathog., 6, 2010, e1001006.
30. Locke, B., Forsgren, E., de Miranda, J.R., Increased tolerance and resistance to virus infections: a possible factor in the survival of Varroa destructor-resistant honey bees (Apis mellifera). PLoS ONE., 9, 2014, e99998.
31. Lough, G., Kyriazakis, I., Bergman, S., Lengeling, A., Doeschl-Wilson, A.B., Health trajectories reveal the dynamic contributions of host genetic resistance and tolerance to infection outcome. Proc. R. Soc. B., 282, 2015 20152151.
32. Mazé-Guilmo, E., Loot, G., Páez, D.J., Lefèvre, T., Blanchet, S., Heritable variation in host tolerance and resistance inferred from a wild host–parasite system. Proc. R. Soc B, 281, 2014 20132567.
33. Medzhitov, R., Schneider, D.S., Soares, M.P., Disease tolerance as a defense strategy. Science 335 (2012), 936–941.
34. Merkling, S.H., Bronkhorst, A.W., Kramer, J.M., Overheul, G.J., Schenck, A., Van Rij, R.P., The epigenetic regulator G9a mediates tolerance to RNA virus infection in Drosophila. PLoS Pathog., 11, 2015, e1004692.
35. Råberg, L., Sim, D., Read, A.F., Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318 (2007), 812–814.
36. Råberg, L., Graham, A.L., Read, A.F., Decomposing health: tolerance and resistance to parasites in animals. Phil. Trans. R. Soc. Lond. B 364 (2009), 37–49.
37. Rausher, M.D., Co-evolution and plant resistance to natural enemies. Nature 411 (2001), 857–864.
38. Regoes, R.R., McLaren, P.J., Battegay, M., Bernasconi, E., Calmy, A., Günthard, H.F., Hoffmann, M., Rauch, A., Telenti, A., Fellay, J., Disentangling human tolerance and resistance against HIV. PLoS Biol., 12, 2014, e1001951.
39. Restif, O., Koella, J.C., Shared control of epidemiological traits in a coevolutionary model of host–parasite interactions. Am. Nat. 161 (2003), 827–836.
40. Restif, O., Koella, J.C., Concurrent evolution of resistance and tolerance to pathogens. Am. Nat. 164 (2004), E90–E102.
41. Rohr, J.R., Raffel, T.R., Hall, C.A., Developmental variation in resistance and tolerance in a multi-host–parasite system. Funct. Ecol. 24 (2010), 1110–1121.
42. Roy, B.A., Kirchner, J.W., Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54 (2000), 51–63.
43. Schmid-Hempel, P., Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics. 2nd ed., 2011, Oxford University Press, Oxford.
44. Schneider, D.S., Tracing personalized health curves during infections. PLoS Biol., 9, 2011, e1001158.
45. Shinzawa, N., Nelson, B., Aonuma, H., Okado, K., Fukumoto, S., Miura, M., Kanuka, H., p38 MAPK-dependent phagocytic encapsulation confers infection tolerance in Drosophila. Cell Host Microbe 6 (2009), 244–252.
46. Simms, E.L., Defining tolerance as a reaction norm. Evol. Ecol. 14 (2000), 563–570.
47. Stearns, S.C., The Evolution of Life Histories. 1992, Oxford University Press, London.
48. Sternberg, E.D., Lefèvre, T., Li, J., de Castillejo, C.L.F., Li, H., Hunter, M.D., de Roode, J.C., Food plant derived disease tolerance and resistance in a natural butterfly–plant–parasite interaction. Evolution 66 (2012), 3367–3376.
49. Sternberg, E.D., Li, H., Wang, R., Gowler, C., de Roode, J.C., Patterns of host–parasite adaptation in three populations of monarch butterflies infected with a naturally occurring protozoan disease: virulence, resistance, and tolerance. Am. Nat. 182 (2013), E235–E248.
50. Vale, P.F., Little, T.J., Fecundity compensation and tolerance to a sterilizing pathogen in Daphnia. J. Evol. Biol. 25 (2012), 1888–1896.
51. Vale, P.F., Fenton, A., Brown, S.P., Limiting damage during infection: lessons from infection tolerance for novel therapeutics. PLoS Biol., 12, 2014, e1001769.
52. Van Hemert, C., Pearce, J.M., Handel, C.M., Wildlife health in a rapidly changing North: focus on avian disease. Front. Ecol. Environ. 12 (2014), 548–556.
53. Vincent, C.M., Sharp, N.P., Sexual antagonism for resistance and tolerance to infection in Drosophila melanogaster. Proc. R. Soc B, 281, 2014, 20140987.