The Effect and Relative Importance of Neutral Genetic Diversity for Predicting Parasitism Varies across Parasite Taxa

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Ruiz López, María José ^a   Monello, Ryan J ^a,b   Gompper, Matthew E ^a   Eggert, Lori S ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b NATIONAL PARK SERVICE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; DERMACENTOR VARIABILIS; ENDOPARASITE; GENE LOCUS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; HETEROZYGOSITY; LOUSE; MICROPARASITE; MICROSATELLITE MARKER; MULTILOCUS SEQUENCE TYPING; NONHUMAN; OUTBRED STRAIN; PARASITISM; POPULATION ABUNDANCE; PREDICTION; RACCOON; SPECIES RICHNESS; TICK; TRICHODECTES OSTOMACULATUS;

ANIMALS; DERMACENTOR; FEMALE; GENETIC HETEROGENEITY; GENETIC LOCI; HETEROZYGOTE; HOST-PARASITE INTERACTIONS; MALE; MICROSATELLITE REPEATS; PHTHIRAPTERA; RACCOONS; SELECTION, GENETIC; SPECIES SPECIFICITY;

DERMACENTOR VARIABILIS; IXODIDA; PHTHIRAPTERA; PROCYON; PROCYON LOTOR; TRICHODECTES OCTOMACULATUS;

EID: 84866863029     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045404     Document Type: Article

References (73)

1. Wilson K, Bjornstad ON, Dobson AP, Merler S, Poglayen G, et al. (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson P J, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP, editors. The Ecology of Wildlife Diseases. Oxford: Oxford University Press. 6-44.
2. Haldane JBS, (1949) Disease and evolution. Ric Sci 19: 68-76.
3. Anderson RM, May RM, (1986) The invasion, persistance and spread of infectious-diseases within animal and plant-communities. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314: 533-570.
4. Côté SD, Stien A, Irvine RJ, Dallas JF, Marshall F, et al. (2005) Resistance to abomasal nematodes and individual genetic variability in reindeer. Mol Ecol 14: 4159-4168.
5. Hawley DM, Sydenstricker KV, Kollias GV, Dhondt AA, (2005) Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches. Biol Lett 1: 326-329.
6. Westerdahl H, Waldenström J, Hansson B, Hasselquist D, von Schantz T, et al. (2005) Associations between malaria and MHC genes in a migratory songbird. Proc R Soc Lond B Biol Sci 272: 1511-1518.
7. Acevedo-Whitehouse K, Spraker TR, Lyons E, Melin SR, Gulland F, et al. (2006) Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups. Mol Ecol 15: 1973-1982.
8. Schwensow N, Fietz J, Dausmann KH, Sommer S, (2007) Neutral versus adaptive genetic variation in parasite resistance: importance of major histocompatibility complex supertypes in a free-ranging primate. Heredity 99: 265-277.
9. Elton CS, (1958). The ecology of invasions by animals and plants. John Wiley: New York. 181 p.
10. Leonard KJ, (1969) Factors affecting rates of stem rust increase in mixed plantings of susceptible and resistant oat varieties cultivars. Phytopathology 59: 1845-1850.
11. Meagher S, (1999) Genetic diversity and Capillaria hepatica (Nematoda) prevalence in Michigan deer mouse populations. Evolution 53: 1318-1324.
12. Poulin R, Marshall LJ, Spencer HG, (2000) Metazoan parasite species richness and genetic variation among freshwater fish species: cause or consequence? Int J Parasitol 30: 697-703.
13. King KC, Lively CM, (2012) Does genetic diversity limit disease spread in natural host populations? Heredity 00: 1-5.
14. MacDougall-Shackleton EA, Derryberry EP, Foufopoulos J, Dobson AP, Hahn TP, (2005) Parasite-mediated heterozygote advantage in an outbred songbird population. Biol Lett 1: 105-107.
15. Piertney SB, Oliver MK, (2005) The evolutionary ecology of the major histocompatibility complex. Heredity 96: 7-21.
16. Spurgin LG, Richardson DS, (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc Lond B Biol Sci 277: 979-988.
17. Bérénos C, Wegner KM, Schmid-Hempel P, (2011) Antagonistic coevolution with parasites maintains host genetic diversity: and experimental test. Proc R Soc Lond B Biol Sci 278: 218-224.
18. Coltman D, Pilkington J, Smith J, Pemberton J, (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53: 1259-1267.
19. Acevedo-Whitehouse K, Gulland F, Greig D, Amos W, (2003) Disease susceptibility in California sea lions. Nature 422: 35-35.
20. Spielman D, Brook BW, Briscoe DA, Frankham R, (2004) Does inbreeding and loss of genetic diversity decrease disease resistance? Conserv Genet 5: 439-448.
21. Ellison A, Cable J, Consuegra S, (2011) Best of both worlds? Association between outcrossing and parasite loads in a selfing fish. Evolution 65: 3021-3026.
22. Weir B, Cockerham C, (1973) Mixed self and random mating at two loci. Genet Res 21: 247-262.
23. David P, (1998) Heterozygosity-fitness correlations: new perspectives on old problems. Heredity 80: 531-537.
24. Szulkin M, Bierne N, David P, (2010) Heterozygosity-fitness correlations: a time for reappraisal. Evolution 64: 1202-1217.
25. Keller L, Waller D, (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17: 230-241.
26. Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC, (2009) A quantitative review of heterozygosity-fitness correlations in animal populations. Mol Ecol 18: 2746-2765.
27. Balloux F, (2004) Heterozygote excess in small populations and the heterozygote-excess effective population size. Evolution 58: 1891-1900.
28. Väli Ü, Einarsson A, Waits L, Ellegren H, (2008) To what extent do microsatellite markers reflect genome-wide genetic diversity in natural populations? Mol Ecol 17: 3808-3817.
29. Ljungqvist M, ÅKesson M, Hansson B, (2010) Do microsatellites reflect genome-wide genetic diversity in natural populations? A comment on Väli,et al. (2008). Mol Ecol 19: 851-855.
30. Hansson B, Westerberg L, (2002) On the correlation between heterozygosity and fitness in natural populations. Mol Ecol 11: 2467-2474.
31. Amos W, Driscoll E, Hoffman JI, (2010) Candidate genes versus genome-wide associations: which are better for detecting genetic susceptibility to infectious disease? Proc R Soc Lond B Biol Sci 278: 1183-1188.
32. Bierne N, Tsitrone A, David P, (2000) An inbreeding model of associative overdominance during a population bottleneck. Genetics 155: 1981-1990.
33. Mueller JC, Hermisson J, Olano-Marin J, Hansson B, Kempenaers B, (2011) Linking genetic mechanisism of heterozygosity fitness correlations to footprints of selection at single loci. Evol Ecol (2011) 25: 1-11.
34. Acevedo-Whitehouse K, Vicente J, Gortazar C, Hofle U, Fernandez-De-Mera I, et al. (2005) Genetic resistance to bovine tuberculosis in the Iberian wild boar. Mol Ecol 14: 3209-3217.
35. Ortego J, Cordero PJ, Aparicio JM, Calabuig G, (2007) No relationship between individual genetic diversity and prevalence of avian malaria in a migratory kestrel. Mol Ecol 16: 4858-4866.
36. Luikart G, Pilgrim K, Visty J, Ezenwa VO, Schwartz MK, (2008) Candidate gene microsatellite variation is associated with parasitism in wild bighorn sheep. Biol Lett 4: 228-231.
37. Rijks JM, Hoffman JI, Kuiken T, Osterhaus A, Amos W, (2008) Heterozygosity and lungworm burden in harbour seals (Phoca vitulina). Heredity 100: 587-593.
38. Ortego J, Aparicio JM, Calabuig G, Cordero PJ, (2007) Risk of ectoparasitism and genetic diversity in a wild lesser kestrel population. Mol Ecol 16: 3712-3720.
39. Monello RJ, Gompper ME, (2007) Biotic and abiotic predictors of tick (Dermacentor variabilis) abundance and engorgement on free-ranging raccoons (Procyon lotor). Parasitology 134: 2053-2062.
40. Monello RJ, Gompper ME, (2009) Relative importance of demographics, locale, and seasonality underlying louse and flea parasitism of raccoons (Procyon lotor). J Parasitol 95: 56-62.
41. Monello RJ, Gompper ME, (2010) Differential effects of experimental increases in sociality on ectoparasites of free-ranging raccoons. J Anim Ecol 79: 602-609.
42. Monello RJ, Gompper ME, (2011) Effects of resource availability and social aggregation on the species richness of raccoon endoparasite infracommunities. Oikos 120: 1427-1433.
43. Wehtje M, Gompper ME, (2011) Effects of an experimentally clumped food resource on raccoon Procyon lotor home-range use. Wildl Biol 17: 25-32.
44. Gompper ME, Monello RJ, Eggert LS, (2011) Genetic variability and viral seroconversion in an outcrossing vertebrate population. Proc R Soc Lond B Biol Sci 278: 204-210.
45. Finkelman FD, Shea-Donohue T, Goldhill J, Sullivan CA, Morris SC, Madden KB, Gause WC, Urban JF Jr, (1997) Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu Rev Immunol 15: 505-533.
46. denHollander N, Allen JR, (1985) Dermacentor variabilis: acquired resistance to ticks in BALB/c mice. Exp Parasitol 59: 118-129.
47. Møller A, Rózsa L, (2005) Parasite biodiversity and host defenses: chewing lice and immune response of their avian hosts. Oecologia 142: 169-176.
48. Lieutenant-Gosselin M, Bertachez L, (2006) Local heterozygosity-fitness correlations with global positive effects on fitness in thresspine stickleback. Evolution 60: 1658-1668.
49. Grau GA, Sanderson GC, Rogers JP, (1970) Age determination in raccoons. J Wildl Manage 266: 215-219.
50. Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ, (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86: 155-163.
51. Eggert LS, Maldonado JE, Fleischer RC (2005) Nucleic acid isolation from ecological samples-Animal scat and other associated materials. In: Zimmer EA, Roalson EH, editors. Methods in Enzymology: Academic Press. 73-82.
52. Siripunkaw C, Kongrit C, Faries KM, Monello RJ, Gompper ME, et al. (2008) Isolation and characterization of polymorphic microsatellite loci in the raccoon (Procyon lotor). Mol Ecol Resour 8: 199-201.
53. Raymond M, Rousset F, (1995) Genepop (version-1.2)- population-genetics software for exact tests and ecumenicism. J Hered 86: 248-249.
54. Excoffier L, Laval G, Scheneider S (2006) Arlequin Ver. 3.1. An Integrated Software Package for Population Genetics Data Analysis.
55. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4: 535-538.
56. Amos W, Wilmer J, Fullard K, (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond B Biol Sci 268: 2021-2027.
57. Aparicio JM, Ortego J, Cordero PJ, (2006) What should we weigh to estimate heterozygosity, alleles or loci? Mol Ecol 15: 4659-4665.
58. Burnham K, Anderson D (2002) Model selection and multimodel inference: A practical information-theoretic approach. New York: Springer-Verlag. 488 p.
59. Neff BD, (2004) Stabilizing selection on genomic divergence in a wild fish population. Proc Natl Acad Sci USA 101: 2381-2385.
60. Slate J, Pemberton J, (2006) Does reduced heterozygosity depress sperm quality in wild rabbits (Oryctolagus cuniculus)? Curr Biol 16: R790-R791.
61. Nakagawa S, Cuthill IC, (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev Camb Philos Soc 82: 591-605.
62. Wielfert L, Schmid-Hempel P. 2008. The genetic architecture of susceptibility to parasites. BMC Evol Biol 8: 187.
63. Spielman D, Brook B, Frankham R, (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101: 15261-15264.
64. Whitaker JOJ, editor (1982) Ectoparasites of mammals of Indiana. Indianapolis: The Indiana Academy of Science. 240 p.
65. Marshall AG, editor (1982) The ecology of ectoparasitic insects. London: Academic Press. 459 p.
66. Whiteman NK, Kimball RT, Parker PG, (2007) Co-phylogeography and comparative population genetics of the threatened Galápagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities. Mol Ecol 16: 4759-4773.
67. Morand S, Krasnov BR, Poulin R, editors (2006) Micromammals and macroparasites: from evolutionary ecology to management. Tokyo: Springer. 647 p.
68. Francischetti IMB, Sá-Nunes A, Mans BJ, Santos IM, Ribeiro JMC, (2009) The role of saliva in tick feeding. Front Biosci 14: 2051-2088.
69. Hovius JWR, (2009) Spitting Image: Tick saliva assists the causative agent of Lyme disease in evading host skin's innate immune response. J Invest Dermatol 129: 2337-2339.
70. Marshall TC, Spalton JA, (2000) Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Anim Conserv 3: 241-248.
71. Thornhill NW, editor (1993) The natural history of inbreeding and outbreeding. Chicago: University of Chicago Press. 584 p.
72. 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.
73. Pitcher TE, Neff BD, (2006) MHC class IIB alleles contribute to both additive an nonadditive genetic effects on survival in Chinook salmon. Mol Ecol 15: 2357-2365.