Heritable variation in host tolerance and resistance inferred from a wild host-parasite system

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1779, 2014, Pages

  Mazé Guilmo, Elise ^a   Loot, Géraldine ^a,b   Páez, David J ^c   Lefèvre, Thierry ^a   Blanchet, Simon ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

Genetic correlation; Host parasite interaction; Long term survey; Molecular based pedigree; Quantitative genetics

Indexed keywords

DEFENSE BEHAVIOR; GENETIC VARIATION; HERITABILITY; HOST RANGE; HOST-PARASITE INTERACTION; POPULATION GENETICS; TOLERANCE; WILD POPULATION;

ANIMAL; ARTICLE; CYPRINIFORMES; DISEASE RESISTANCE; GENETIC CORRELATION; GENETIC VARIABILITY; GENETICS; GENOTYPE; HOST PARASITE INTERACTION; HOST-PARASITE INTERACTION; LONG-TERM SURVEY; MOLECULAR-BASED PEDIGREE; PARASITOLOGY; QUANTITATIVE GENETICS;

GENETIC CORRELATION; HOST-PARASITE INTERACTION; LONG-TERM SURVEY; MOLECULAR-BASED PEDIGREE; QUANTITATIVE GENETICS;

ANIMALS; CYPRINIDAE; DISEASE RESISTANCE; GENETIC VARIATION; GENETICS; GENOTYPE; HOST-PARASITE INTERACTIONS; PARASITOLOGY;

EID: 84893077630     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2013.2567     Document Type: Article

References (59)

1. Roy BA, Kirchner JW. 2000 Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54, 51-63. (doi:10.1111/j.0014-3820.2000.tb00007.x)
2. Miller MR, Whiten A, Boots M. 2005 The evolution of host resistance: tolerance and control as distinct strategies. J. Theor. Biol. 236, 198-207. (doi:10. 1016/j.jtbi.2005.03.005)
3. Raoberg L, Graham AL, Read AF. 2009 Decomposing health: tolerance and resistance to parasites in animals. Phil. Trans. R. Soc. B 364, 37-49. (doi:10. 1098/rstb.2008.0184)
4. Medzhitov R, Schneider DS, Soares MP. 2012 Disease tolerance as a defense strategy. Science 335, 936-941. (doi:10.1126/science.1214935)
5. Baucom RS, de Roode JC. 2011 Ecological immunology and tolerance in plants and animals. Funct. Ecol. 25, 18-28. (doi:10.1111/j.1365-2435. 2010.01742.x)
6. Ayres JS, Schneider DS. 2012 Tolerance of Infections. Annu. Rev. Immunol. 30, 271-294. (doi:10.1146/ annurev-immunol-020711-075030)
7. Little TJ, Shuker DM, Colegrave N, Day T, Graham AL. 2010 The coevolution of virulence: tolerance in perspective. PLoS Pathog. 6, e1001006. (doi:10.1371/ journal.ppat.1001006)
8. Wolinska J, King KC. 2009 Environment can alter selection in host-parasite interactions. Trends Parasitol. 25, 236-244. (doi:10.1016/j.pt.2009. 02.004)
9. Boots M, Best A, Miller MR, White A. 2009 The role of ecological feedbacks in the evolution of host defence: what does theory tell us? Phil. Trans. R. Soc. B 364, 27-36. (doi:10.1098/rstb. 2008.0160)
10. Best A, White A, Boots M. 2008 Maintenance of host variation in tolerance to pathogens and parasites. Proc. Natl Acad. Sci. USA 105, 20 786-20 791. (doi:10.1073/pnas.0809558105)
11. Raoberg L, Sim D, Read AF. 2007 Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318, 812-814. (doi:10.1126/science.1148526)
12. Ayres JS, Schneider DS. 2009 The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biol. 7, e1000150. (doi:10.1371/journal. pbio.1000150)
13. Ayres JS, Freitag N, Schneider DS. 2008 Identification of Drosophila mutants altering defense of and endurance to listeria monocytogenes infection. Genetics 178, 1807-1815.
14. Blanchet S, Rey F, Loot G. 2010 Evidence for host variation in parasite tolerance in a wild fish population. Evol. Ecol. 24, 1129-1139. (doi:10. 1007/s10682-010-9353-x)
15. Lefevre T, Williams AJ, de Roode JC. 2011 Genetic variation in resistance, but not tolerance, to a protozoan parasite in the monarch butterfly. Proc. R. Soc. B 278, 751-759. (doi:10.1098/rspb.2010.1479)
16. Carval D, Ferriere R. 2010 A unified model for the coevolution of resistance, tolerance, and virulence. Evolution 64, 2988-3009. (doi:10.1111/j.1558-5646.2010.01035.x)
17. Fornoni J, Valverde PL, Nunez-Farfan J. 2003 Quantitative genetics of plant tolerance and resistance against natural enemies of two natural populations of Datura stramonium. Evolution 5, 1049-1065.
18. Juenger T, Bergelson J. 2000 The evolution of compensation to herbivory in scarlet gilia, Ipomopsis aggregata: herbivore-imposed natural selection and the quantitative genetics of tolerance. Evolution 54, 764-777.
19. Falconer DS, MacKay TFC. 1996 Introduction to quantitative genetics, 4th edn. Harlow, UK: Prentice Hall.
20. Danchin E, Charmantier A, Champagne FA, Mesoudi A, Pujol B, Blanchet S. 2011 Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat. Rev. Genet. 12, 475-486. (doi:10.1038/nrg3028)
21. Bonduriansky R, Day T. 2009 Nongenetic inheritance and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 40, 103-125. (doi:10.1146/annurev. ecolsys.39.110707.173441)
22. Fineblum WL, Rausher MD. 1995 Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377, 517-520. (doi:10.1038/ 377517a0)
23. Blanchet S, Rey O, Berthier P, Lek S, Loot G. 2009 Evidence of parasite-mediated disruptive selection on genetic diversity in a wild fish population. Mol. Ecol. 18, 1112-1123.
24. Wilson AJ, Reale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH. 2010 An ecologist's guide to the animal model. J. Anim. Ecol. 79, 13-26. (doi:10.1111/j.1365-2656.2009.01639.x)
25. Sternberg ED, Lefèvre T, Li J, de Castillejo CLF, Li H, Hunter MD, de Roode JC. 2012 Food plant derived disease tolerance and resistance in a natural butterfly-plant-parasite interactions. Evolution 66, 3367-3376. (doi:10.1111/j.1558-5646.2012.01693.x)
26. Lootvoet A, Blanchet S, Gevrey M, Buisson L, Tudesque L, Loot G. 2013 Patterns and processes of alternative host use in a generalist parasite: insights from a natural host-parasite interaction. Funct. Ecol. 27, 1403-1414. (doi:10.1111/1365-2435.12140)
27. Loot G, Poulet N, Reyjol Y, Blanchet S, Lek S. 2004 The effects of the ectoparasite Tracheliastes polycolpus (Copepoda: Lernaeopodidae) on the fins of rostrum dace (Leuciscus leuciscus burdigalensis). Parasitol. Res. 94, 16-23. (doi:10.1007/s00436-004-1166-9)
28. Blanchet S, Mejean L, Bourque JF, Lek S, Thomas F, Marcogliese DJ, Dodson J, Loot G. 2009 Why parasitized hosts look different? Resolving the 'chicken-egg' dilemma. Oecologia 160, 37-47.
29. Corby-Harris V, Habel KE, Ali FG, Promislow DEL. 2007 Alternative measures of response to Pseudomonas aeruginosa infection in Drosophila melanogaster. J. Evol. Biol. 20, 526-533. (doi:10. 1111/j.1420-9101.2006.01267.x)
30. Blanchet S, Rey O, Etienne RS, Lek S, Loot G. 2010 Species-specific responses to landscape fragmentation: implications for management strategies. Evol. Appl. 3, 291-304.
31. Cardon M, Loot G, Grenouillet G, Blanchet S. 2011 Host characteristics and environmental factors differentially drive the burden and pathogenicity of an ectoparasite: a multilevel causal analysis. J. Anim. Ecol. 80, 657-667. (doi:10.1111/j.1365-2656.2011.01804.x)
32. Harrison EC, Saenz-Agudelo P, Planes S, Jones GP, Berumen ML. 2013 Relative accuracy of three common methods of parentage analysis in natural populations. Mol. Ecol. 22, 1158-1170. (doi:10. 1111/mec.12138)
33. Wilberg MJ, Dreher BP. 2004 GENECAP: a program for analysis of multilocus genotype data for noninvasive sampling and capture-recapture population estimation. Mol. Ecol. Notes 4, 783-785. (doi:10. 1111/j.1471-8286.2004.00797.x)
34. Herbinger C. 2005 Pedigree 2.2 help manual. See http://herbinger.biology.dal.ca:5080/Pedigree.
35. Herbinger CM, O'Reilly PT, Verspoor E. 2006 Unravelling first-generation pedigrees in wild endangered salmon populations using molecular genetic markers. Mol. Ecol. 15, 2261-2275.
36. Andersson EC, Dunham KK. 2005 spip 1.0: a program for simulating pedigrees and genetic data in agestructured populations. Mol. Ecol. Notes 5, 459-461. (doi:10.1111/j.1471-8286.2005.00884.x)
37. Coombs JA, Letcher BH, Nislow KH. 2010 PedAgree: software to quantify error and assess accuracy and congruence for genetically reconstructed pedigree relationships. Conserv. Genet. Resour. 2, 147-150. (doi:10.1007/s12686-010-9202-9)
38. Hadfield JD. 2010 MCMC methods for multiresponse generalised linear mixed models: the MCMCglmm R package. J. Stat. Soft. 33, 1-22.
39. Nakagawa S, Schielzeth H. 2010 Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. 85, 935-956. (doi:10.1111/ j.1469-185X.2010.00141.x)
40. Koskela T, Puustinen S, Salonen V, Mutikainen P. 2002 Resistance and tolerance in a host plant-holoparasitic plant interaction: genetic variation and costs. Evolution 56, 899-908.
41. Boulinier T, Sorci G, Monnat J-Y, Danchin E. 1997 Parent-offspring regression suggests heritable susceptibility to ectoparasites in a natural population of kittiwake Rissa tridactyla. J. Evol. Biol. 10, 77-85. (doi:10.1046/j.1420-9101.1997. 10010077.x)
42. Smith JA, Wilson K, Pilkington JG, Pemberton JM. 1999 Heritable variation in resistance to gastrointestinal nematodes in an unmanaged mammal population. Proc. R. Soc. Lond. B 266, 1283-1290. (doi:10.1098/rspb.1999.0776)
43. Uller T, Olsson M, Madsen T. 2003 Family and population effects on disease resistance in a reptile. Heredity 91, 112-116. (doi:10.1038/sj.hdy. 6800288)
44. Kover PX, Schaal BA. 2002 Genetic variation for disease resistance and tolerance among Arabidopsis thaliana accessions. Proc. Natl Acad. Sci. USA 99, 11 270-11 274. (doi:10.1073/pnas.102288999)
45. Anderson JT, Lee C-R, Rushworth CA, Colautti RI, Mitchell-Olds T. 2013 Genetic trade-offs and conditional neutrality contribute to local adaptation: genetic basis of local adaptation. Mol. Ecol. 22, 699-708. (doi:10.1111/j.1365-294X.2012.05522.x)
46. Carlson SM, Seamons TR. 2008 A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change. Evol. Appl. 1, 222-238.
47. Kube PD, Taylor RS, Elliott NG. 2012 Genetic variation in parasite resistance of Atlantic salmon to amoebic gill disease over multiple infections. Aquaculture 364-365, 165-172. (doi:10.1016/j. aquaculture.2012.08.026)
48. Kause A, van Dalen S, Bovenhuis H. 2012 Genetics of Ascites resistance and tolerance in chicken: a random regression approach. Genes Genomes Genet. 2, 527-535. (doi:10.1534/g3. 112.002311)
49. Thomas SC, Hill WG. 2000 Estimating quantitative genetic parameters using sibships reconstructed from marker data. Genetics 155, 1961-1972.
50. Restif O, Koella JC. 2004 Concurrent evolution of resistance and tolerance to pathogens. Am. Nat. 164, E90-E102. (doi:10.1086/423713)
51. Mauricio R, Rausher MD, Burdick DS. 1997 Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78, 1301-1311. (doi:10.1890/0012-9658(1997)078 [1301:VITDSO]2.0.CO;2)
52. Simms EL, Triplett J. 1994 Costs and benefits of plant-responses to disease: resistance and tolerance. Evolution 48, 1973-1985. (doi:10.2307/2410521)
53. Sgrò CM, Hoffmann AA. 2004 Genetic correlations, tradeoffs and environmental variation. Heredity 93, 241-248. (doi:10.1038/sj.hdy.6800532)
54. Laine A-L. 2008 Temperature-mediated patterns of local adaptation in a natural plant-pathogen metapopulation. Ecol. Lett. 11, 327-337. (doi:10. 1111/j.1461-0248.2007.01146.x)
55. Stopher KV, Walling CA, Morris A, Guinness FE, Clutton-Brock TH, Pemberton JM, Nussey DH. 2012 Shared spatial effects on quantitative genetic parameters: accounting for spatial autocorrelation and home range overlap reduces estimates of heritability in wild red deer. Evolution 66, 2411-2426. (doi:10.1111/j.1558-5646.2012.01620.x)
56. Gómez-Di{dotless}́az E, Jordà M, Peinado MA, Rivero A. 2012 Epigenetics of host-pathogen interactions: the road ahead and the road behind. PLoS Pathog. 8, e1003007. (doi:10.1371/journal.ppat.1003007)
57. Gasparini J, McCoy KD, Haussy C, Tveraa T, Boulinier T. 2001 Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proc. R. Soc. Lond. B 268, 647-650. (doi:10.1098/rspb.2000.1411)
58. Roff DA. 1996 The evolution of genetic correlations: an analysis of patterns. Evolution 50, 1392-1403. (doi:10.2307/2410877)
59. Thrall PH, Laine A-L, Ravensdale M, Nemri A, Dodds PN, Barrett LG, Burdon JJ. 2012 Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation: coevolution in a wild host-pathogen system. Ecol. Lett. 15, 425-435. (doi:10.1111/j.1461-0248.2012.01749.x)