Is there sex-biased resistance and tolerance in Mediterranean wood mouse (Apodemus sylvaticus) populations facing multiple helminth infections?

Oecologia

Volumn 170, Issue 1, 2012, Pages 123-135

  Bordes, Frédéric ^a   Ponlet, Nicolas ^a   de Bellocq, Joëlle Goüy ^c,d   Ribas, Alexis ^e   Krasnov, Boris R ^f   Morand, Serge ^a,b  

^a CNRS   (France)

^b CIRAD   (France)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d INSTITUTE OF VERTEBRATE BIOLOGY   (Czech Republic)

^e UNIVERSITY OF BARCELONA   (Spain)

^f BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Apodemus sylvaticus; Body condition; Helminths; Parasites; PHA; Resistance; Sexual dimorphism; Spleen; Testes mass; Tolerance

Indexed keywords

BODY CONDITION; CORRELATION; IMMUNE RESPONSE; INFECTIOUS DISEASE; MEDITERRANEAN ENVIRONMENT; PARASITE INFESTATION; PHYLOGEOGRAPHY; QUANTITATIVE ANALYSIS; RODENT; SEXUAL DIMORPHISM;

ADAPTATION; ANIMAL; ARTICLE; FEMALE; HELMINTH; HOST PARASITE INTERACTION; IMMUNOLOGY; MALE; MURINAE; ORGAN SIZE; PARASITOLOGY; PATHOGENICITY; REPRODUCTION; SEX DIFFERENCE; SPLEEN; THEORETICAL MODEL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; FEMALE; HELMINTHS; HOST-PARASITE INTERACTIONS; MALE; MODELS, THEORETICAL; MURINAE; ORGAN SIZE; REPRODUCTION; SEX FACTORS; SPLEEN;

ANIMALIA; APODEMUS SYLVATICUS; VERMES;

EID: 84865580882     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-012-2300-5     Document Type: Article

References (95)

1. Adamczewska-Andrezejwska KA (1967) Age reference model for Apodemus flavicollis (Melchior, 1834). Ekologia Polska 15: 788-790.
2. Ali NM, Behnke JM (1985) Observations on the gross changes in the secondary lymphoid organs of mice infected with Nematospiroides dubius. J Helminthol 59: 167-174.
3. Arneberg P (2002) Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25: 88-94.
4. Attuquayefio DK, Gorman ML, Wolton RJ (1985) Home range sizes in the wood mouse Apodemus sylvaticus: habitat, sex and seasonal differences. J Zool 210: 45-53.
5. Bateman A (1948) Intrasexual selection in Drosophila. Heredity 2: 349-368.
6. Baucom RS, de Roode JC (2011) Ecological immunology and tolerance in plants and animals. Func Ecol 25: 18-28.
7. Behnke JM, Lewis JW, Zain SN, Gilbert FS (1999) Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. J Helminthol 73: 31-44.
8. Beldomenico PM, Telfer S, Gebert S, Lukomski L, Bennett M, Begon M (2008) Poor condition and infection: a vicious circle in natural populations. Proc R Soc London B 275: 1753-1759.
9. Beldomenico PM, Telfer S, Lukomski L, Gebert S, Bennett M, Begon M (2009a) Host condition and individual risk of cowpox virus infection: cause or effect? Epidermiol Infect 137: 1295-1301.
10. Beldomenico PM, Telfer S, Gebert S, Lukomski L, Bennett M, Begon M (2009b) The vicious circle and infection intensity: the case of Trypanosoma microti in field vole populations. Epidemics 1: 162-167.
11. Bize P, Jeanneret C, Klopfenstein A, Roulin A (2008) What makes a host profitable? Parasites balance host nutritive resources against immunity. Am Nat 171: 107-118.
12. Blanchet S, Rey O, Loot G (2010) Evidence for host variation in parasite tolerance in a wild fish population. Evol Ecol 24: 1129-1139.
13. Bordes F, Morand S (2009) Parasite diversity: an overlooked metric of parasite pressures? Oikos 118: 801-806.
14. Bordes F, Morand S, Kelt DA, van Vuren DH (2009) Home range and parasite diversity in mammals. Am Nat 173: 467-474.
15. Boughton RK, Joop G, Armitage SAO (2011) Outdoor immunology: methodological considerations for ecologists. Func Ecol 25: 81-100.
16. Bradley J, Jackson JA (2008) Measuring immune system variation to help understand host-pathogen community dynamics. Parasitology 135: 1-17.
17. Brown CR, Brown MB (2002) Spleen volume varies with colony size and parasite load in a colonial bird. Proc R Soc London B 269: 1367-1373.
18. Clarke D (1986) Tolerance of parasites and diseases in plants and its significance in host-parasite interactions. Adv Plant Pathol 5: 161-197.
19. Cowan KM, Shutler D, Herman TB, Stewart DT (2007) Extreme male biased infections of masked shrews by bladder nematodes. J Mam 88: 1539-1543.
20. Cowan KM, Shutler D, Herman TB, Stewart DT (2009) Splenic mass of masked shrews, Sorex cinereus, in relation to body mass, sex, age, day of the year and bladder nematode, Liniscus (=Capillaria) maseri, infection. J Parasitol 95: 228-230.
21. Cox RM, Parker EU, Cheney DM et al (2010) Experimental evidence for physiological costs underlying the trade-off between reproduction and survival. Func Ecol 24: 1262-1269.
22. Demas GE, Zysling DA, Beecher BR, Muehlenbein MP, French SS (2011) Beyond phytohaemaglutinin: assessing vertebrate immune function across ecological contexts. J Anim Ecol 80: 710-730.
23. Dick CW, Gannon MR, Little WE, Patrick MJ (2003) Ectoparasite associations of bats from central Pennsylvania. J Med Entomol 40: 813-819.
24. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125: 1-15.
25. Ferrari N, Cattadori IM, Nespereira J, Rizzoli A, Hudson PJ (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Lett 7: 88-94.
26. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139: 603-622.
27. French SS, de Nardo DF, Moore MC (2007) Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? Am Nat 170: 79-89.
28. Fuentes MV, Saez S, Trelis M, Galan-Puchades MT, Esteban JG (2004) The helminth community of the wood mouse, Apodemus sylvaticus in the Sierra Espuna Murcia, Spain. J Helminthol 78: 219-223.
29. Fumagalli M, Pozzoli U, Cagliani R, Comi GP et al (2009) Parasites represent a major selective force for interleukine genes and shape the genetic predisposition to autoimmune conditions. J Exp Med 206: 1395-1408.
30. Fumagalli M, Pozzoli U, Cagliani R, Comi GP et al (2010) The landscape of human genes involved in the immune response to parasitic worms. BMC Evol Biol 10: 264.
31. Goüy de Bellocq J, Sarà M, Casanova JC, Feliu C, Morand S (2003) A comparison of the structure of helminth communities of the wild woodmouse, Apodemus sylvaticus on islands of the Western Mediterranean and continental Europe. Parasitol Res 90: 64-70.
32. Goüy de Bellocq J, Ribas A, Casanova JC, Morand S (2007) Immunocompetence and helminth community of the white-toothed shrew, Crocidura russula from the Montseny Natural Park, Spain. Eur J Wild Res 53: 315-320.
33. Graham AL, Hayward AD, Watt KA, Pilkington JG, Pemberton JM, Nussey DH (2010) Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330: 662-665.
34. Harrison A, Scantlebury M, Montgomery WI (2010) Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 119: 1099-1104.
35. Hillegass MA, Waterman JM, Roth JD (2008) The influence of sex and sociality on parasite loads in an African ground squirrel. Behav Ecol 19: 1006-1011.
36. Hoby S, Scharzenberger F, Doherr MG, Robert N, Walzer C (2006) Steroid hormone related male biased parasitism in chamois, Rupicapra rupicapra rupicapra. Vet Parasitol 138: 337-348.
37. Horak P, Tummelecht L, Talvik H (2006) Predictors and markers of resistance to neurotropic nematode infection in rodent host. Parasitol Res 98: 396-402.
38. Jackson JA, Begon M, Birtles R et al (2011) The analysis of immunological profiles in wild animals: a case study on immunodynamics in the field vole, Microtus agrestis. Mol Ecol 20: 893-909.
39. Kanuch P, Kristin A, Kristofik J (2005) Phenology, diet, and ectoparasites of Leisler's bat (Nyctalus leisleri) in the western Carpathians (Slovakia). Acta Chiropterologica 7: 249-257.
40. Kennedy MV, Nager R (2006) The perils and prospects of using phytohaemagglutinin in evolutionary ecology. Trends Ecol Evol 21: 653-655.
41. Khokhlova IS, Krasnov BR, Kam M, Burdelova NI, Degen AA (2002) Energy cost of ectoparasitism: the flea Xenopsylla ramesis on the desert gerbil Gerbillus dasyurus. J Zool 258: 349-354.
42. Kiffner C, Vor T, Hagedorn P, Niedrig M, Ruhe F (2011) Factors affecting patterns of tick parasitism on forest rodents in tick-borne encephalitis risk areas, Germany. Parasitol Res 108: 323-335.
43. Klein SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26: 247-264.
44. Klein SL, Nelson RJ (1998) Adaptative immune responses are linked to the mating system of arvicoline rodents. Am Nat 151: 59-67.
45. Krasnov BR, Morand S, Hawlena H, Khokhlova I, Shenbrot GI (2005) Sex biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146: 209-217.
46. Krasnov BR, Bordes F, Khokhlova IS, Morand S (2012) Gender-biased parasitism in small mammals: patterns, mechanisms, consequences. Mammalia (in press).
47. Lefebvre F, Mounaix B, Poizat G, Crivelli AJ (2004) Impacts of the swimbladder nematode Anguillicola crassus on Anguilla anguilla: variations in liver and spleen masses. J Fish Biol 64: 435-447.
48. Lefèvre T, Williams AO, Roode JC (2011) Genetic variation in resistance but not tolerance, to a protozoan parasite in the monarch butterfly. Proc R Soc Lond B 278: 751-759.
49. Leitner G, Heller D, Friedman A (1989) Sex-related differences in immune response and survival rate of broiler chickens. Vet Immunol Immunopathol 21: 249-260.
50. Limaye N, Blobrajdic KA, Wandstrat AE, Bonhomme F, Edwards SV, Wakeland EK (2008) Prevalence and evolutionary origins of autoimmune susceptibility alleles in natural mouse populations. Genes Immun 9: 61-68.
51. Lindström KM, Foufopoulos J, Pärn H, Wikelski M (2004) Immunological investments reflect parasite abundance in island populations of Darwin's finches. Proc R Soc London B 271: 1513-1519.
52. Lochmiller RL, Derenberg C (2000) Trade-offs in evolutionary ecology: just what is the cost of immunity? Oikos 88: 87-98.
53. Lynch M (1991) Methods for the analysis of comparative data in evolutionary biology. Evolution 45: 1065-1080.
54. Ma Y, Seiler KP, Eichwald EJ, Weis JH, Teuscher C, Weis JJ (1998) Distinct characteristics of resistance to Borrelia burgdorferi-induced arthritis in C57BL/6 N mice. Infect Immun 66: 161-168.
55. Malo AF, Roldan ERS, Garde JJ, Soler AJ, Vicente J, Gortazar C, Gomendio M (2009) What does testosterone do for red deer males? Proc R Soc Lond B 276: 971-980.
56. Martin LB, Wiel ZM, Nelson RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Phil Trans R Soc Lond B 363: 321-339.
57. Michaux J, Goüy de Bellocq J, Sara M, Morand S (2002) Body size increase in insular rodent populations: a role for predators? Glob Ecol Biogeogr 11: 427-436.
58. Milazzo C, Di Bella C, Casanova JC, Ribas A, Cagnin M (2010) Helminth communities of wood mouse (Apodemus sylvaticus) on the River Avena (Calabria), Southern Italy). Hystrix Italian J Mam 21: 171-176.
59. Mills SC, Grapputo A, Jokinen I, Koskela E, Mappes T, Oksanen TA, Poikonen T (2009) Testosterone-mediated effects on fitness-related phenotypic traits and fitness. Am Nat 173: 475-487.
60. Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297: 2015-2018.
61. Morand S, Goüy de Bellocq J, Stanko M, Miklisová D (2004) Is sex-biased ectoparasitism related to sexual size dimorphism in small mammals of central Europe? Parasitology 129: 505-510.
62. Munyeme M, Munang'andu HM, Muma JB, Nambota AM, Biffa D, Siamudaala VM (2011) Investigating effects of parasite infection on body condition of the Kafue lechwe (Kobus leche kafuensis) in the Kafue basin. BMC Res Notes 3: 346.
63. Navarro-Gonzalez N, Verheyden H, Hoste H, Cargnelutti B, Lourtet B, Merlet J, Daufresne T, Lavín S, Hewison AJM, Morand S, Serrano E (2010) Diet quality and immunocompetence influence parasite load of roe deer in a fragmented landscape. Eur J Wild Res 57: 639-645.
64. Nieberding C, Morand S, Libois R, Michaux JR (2004) A parasite reveals cryptic phylogeographic history of its host. Proc R Soc London B 271: 2559-2568.
65. Nunn CL, Lindenfors P, Pursall ER, Rolff J (2009) On sexual dimorphism in immune function. Phil Trans R Soc Lond B 364: 61-69.
66. Pap PL, Czirjak GA, Vagasi SI, Barta Z, Hasselquist DS (2010) Sexual dimorphism in immune function changes during the annual cycle in house sparrows. Naturwissenschaften 97: 891-901.
67. Parapanov RN, Nusslé S, Crausaz M, Senn A, Hausser J, Vogel P (2009) Testis size, sperm characteristics and testosterone concentrations in four species of shrews (Mammalia, Soricidae). Anim Reprod Sci 114: 269-278.
68. Patterson BD, Dick CW, Dittmar K (2008) Sex biases in parasitism of neotropical bats by bat flies (Diptera: Streblidae). J Trop Ecol 24: 387-396.
69. Pedersen AB, Babayan SA (2011) Wild immunology. Mol Ecol 20: 872-880.
70. Peig J, Green AJ (2010) The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Func Ecol 24: 1323-1332.
71. Perez-Orella C, Schulte-Hostedde AI (2005) Effects of sex and body size on ectoparasite loads in the northern flying squirrel (Glaucomys sabrinus). Can J Zool 83: 1381-1385.
72. Pinheiro JC, Bates DM (2000) Mixed effect models in S and S-plus. Springer, New York.
73. Pinzan CF, Ruas LP, Casabona-Fortunado AS et al (2010) Immunological basis for the gender differences in murine Paracoccidioides brasiliensis infection. PLoS ONE 55: 10757.
74. Ponlet N, Chaisiri K, Claude J, Morand S (2011) Incorporating parasite systematic in comparative analyses of variation in spleen mass and testes sizes of rodents. Parasitology 138: 1804-1814.
75. Poulin R (1996) Sexual inequalities in helminth infections: a cost of being male? Am Nat 147: 287-295.
76. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, http://www. R-project. org.
77. Råberg L, Sim D, Read AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318: 812-814.
78. Råberg L, Graham AL, Read AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Phil Trans R Soc Lond B 364: 37-49.
79. Roberts ML, Buchanna KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68: 227-239.
80. Rohr JS, Raffel TR, Hall CA (2010) Developmental variation in resistance and tolerance in a multi-host-parasite system. Func Ecol 24: 1110-1121.
81. Rolff J (2002) Bateman's principle and immunity. Proc R Soc Lond B 269: 867-872.
82. Sak L, Karu U, Horak P (2006) Do standard measures of immunocompetence reflect parasite resistance? The case of greenfinch coccidiosis. Func Ecol 20: 75-82.
83. Sanchez A, Devevey G, Bize P (2011) Female-biased infection and transmission of the gastrointestinal nematode Trichuris arvicolae infecting the common vole Microtus arvalis. Int J Parasitol 41: 1397-1402.
84. Scantlebury M, McWilliams MM, Marks NJ, Dick JTA, Edgar H, Lutermann H (2010) Effects of life-history traits on parasite load in grey squirrels. J Zool 282: 246-255.
85. Schneider DS, Ayres J (2008) Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nature Rev 8: 889-895.
86. Schulte-Hostedde AI, Elsasser SC (2011) Spleen mass, body condition, and parasite loads in male American mink (Neovison vison). J Mammal 92: 221-226.
87. Skorping A, Jensen KH (2004) Disease dynamics: all caused by males? Trends Ecol Evol 19: 219-220.
88. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immuno-competence. Func Ecol 13: 567-572.
89. Tella JL, Lemus JA, Carrete M, Blanco G (2008) The PHA test reflects acquired T-cell mediated immunocompetence in birds. Plos One 3: e3295.
90. Tschirren B, Fitze PS, Richner H (2003) Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. J Anim Ecol 72: 839-845.
91. Vicente J, Pérez-Rodríguez L, Gortázar C (2007) Sex, age, spleen size, and kidney fat of red deer relative to infection intensities of the lungworm Elaphostrongylus cervi. Naturwissenschaften 94: 581-587.
92. Waterman J (2007) Male mating strategies. In: Wolf JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. The University of Chicago Press, Chicago, pp 27-41.
93. Wauters LA, Dhondt AA (1995) Lifetime reproductive success and its correlates in female Eurasian red squirrels. Oikos 72: 402-410.
94. Wilson K, Moore SL, Owens IPF (2003) Response to comment on "Parasites as a viability cost of sexual selection in natural populations of mammals". Science 300: 55.
95. Zuk M (2009) The sicker sex. PLoS Pathog 5: e1000267.