Conservation Genetics

, Volume 11, Issue 5, pp 2001–2013

Variety matters: adaptive genetic diversity and parasite load in two mouse opossums from the Brazilian Atlantic forest

  • Yvonne Meyer-Lucht
  • Celine Otten
  • Thomas Püttker
  • Renata Pardini
  • Jean Paul Metzger
  • Simone Sommer
Research Article

Abstract

The adaptive potential of a species to a changing environment and in disease defence is primarily based on genetic variation. Immune genes, such as genes of the major histocompatibility complex (MHC), may thereby be of particular importance. In marsupials, however, there is very little knowledge about natural levels and functional importance of MHC polymorphism, despite their key role in the mammalian evolution. In a previous study, we discovered remarkable differences in the MHC class II diversity between two species of mouse opossums (Gracilinanus microtarsus, Marmosops incanus) from the Brazilian Atlantic forest, which is one of the most endangered hotspots for biodiversity conservation. Since the main forces in generating MHC diversity are assumed to be pathogens, we investigated in this study gastrointestinal parasite burden and functional associations between the individual MHC constitution and parasite load. We tested two contrasting scenarios, which might explain differences in MHC diversity between species. We predicted that a species with low MHC diversity would either be under relaxed selection pressure by low parasite diversity (‘Evolutionary equilibrium’ scenario), or there was a recent loss in MHC diversity leading to a lack of resistance alleles and increased parasite burden (‘Unbalanced situation’ scenario). In both species it became apparent that the MHC class II is functionally important in defence against gastrointestinal helminths, which was shown here for the first time in marsupials. On the population level, parasite diversity did not markedly differ between the two host species. However, we did observe considerable differences in the individual parasite load (parasite prevalence and infection intensity): while M. incanus revealed low MHC DAB diversity and high parasite load, G. microtarsus showed a tenfold higher population wide MHC DAB diversity and lower parasite burden. These results support the second scenario of an unbalanced situation.

Keywords

Neotropical marsupials Marmosops incanus Gracilinanus microtarsus Mata Atlântica Major histocompatibility complex Pathogen-driven selection 

Supplementary material

10592_2010_93_MOESM1_ESM.doc (42 kb)
Supplementary material 1 (DOC 42 kb)
10592_2010_93_MOESM2_ESM.doc (48 kb)
Supplementary material 2 (DOC 48 kb)

References

  1. Abu-Madi MA, Behnke JM, Lewis JW, Gilbert FS (2000) Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. J Helminthol 74:7–15PubMedGoogle Scholar
  2. Altizer S, Harvell D, Friedle E (2003) Rapid evolutionary dynamics and disease threats to biodiversity. Trends Ecol Evol 18:589–596CrossRefGoogle Scholar
  3. Altizer S, Nunn CL, Lindenfors P (2007) Do threatened hosts have fewer parasites? A comparative study in primates. J Anim Ecol 76:304–314CrossRefPubMedGoogle Scholar
  4. Apanius V, Penn D, Slev P, Ruff L, Potts W (1997) The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179–224PubMedGoogle Scholar
  5. Behnke JM, Barnard CJ, Bajer A, Bray D, Dinmore J, Frake K, Osmond J, Race T, Sinski E (2001) Variation in the helminth community structure in bank voles (Clethrionomys glareolus) from three comparable localities in the Mazury Lake District region of Poland. Parasitology 123:401–414CrossRefPubMedGoogle Scholar
  6. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16:363–377CrossRefPubMedGoogle Scholar
  7. Bowen L, Aldridge BM, Gulland F, Van Bonn W, DeLong R, Melin S, Lowenstine LJ, Stott JL, Johnson ML (2004) Class II multiformity generated by variable MHC-DRB region configurations in the California sea lion (Zalophus californianus). Immunogenetics 56:12–27CrossRefPubMedGoogle Scholar
  8. Brown JL, Erklund A (1994) Kin recognition and the major histocompatibility complex: an integrative review. Am Nat 143:435–461CrossRefGoogle Scholar
  9. Brown JH, Jardetzky TS, Gorga JC, Stern LJ (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364:33–39CrossRefPubMedGoogle Scholar
  10. Caceres NC (2004) Diet of three didelphid marsupials (Mammalia, Didelphimorphia) in southern Brazil. Mamm Biol 69:430–433CrossRefGoogle Scholar
  11. Cassinello J, Gomendio M, Roldan E (2001) Relationship between coefficient of inbreeding and parasite burden in endangered gazelles. Conserv Biol 15:1171–1174CrossRefGoogle Scholar
  12. Coltman D, Pilkington J, Smith J, Pemberton J (1999) Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evolution 53:1259–1267CrossRefGoogle Scholar
  13. Cunha AA, Vieira MV (2002) Support diameter, incline, and vertical movements of four didelphid marsupials in the Atlantic forest of Brazil. J Zool 258:419–426CrossRefGoogle Scholar
  14. Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50–52CrossRefPubMedGoogle Scholar
  15. Dorman SE, Hatem CL, Tyagi S, Aird K, Lopez-Molina J, Pitt MLM, Zook BC, Dannenberg AM Jr., Bishai WR, Manabe YC (2004) Susceptibility to tuberculosis: clues from studies with inbred and outbred New Zealand white rabbits. Infect Immun 72:1700–1705CrossRefPubMedGoogle Scholar
  16. Doxiadis GGM, Otting N, de Groot NG, Noort R, Bontrop RE (2000) Unprecedented polymorphism of MHC-DRB region configurations in Rhesus Macaques. J Immunol 164:3193–3199PubMedGoogle Scholar
  17. Doytchinova IA, Flower DR (2005) In silico identification of supertypes for class II MHCs. J Immunol 174:7085–7095PubMedGoogle Scholar
  18. Ferrari N, Cattadori I, Nespereira J, Rizzoli A, Hudson P (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Lett 7:88–94CrossRefGoogle Scholar
  19. Fonseca GAB, Kierulff MCM (1989) Biology and natural history of Brazilian Atlantic forest small mammals. Bull Fla State Mus Biol Sci 34:99–152Google Scholar
  20. Froeschke G, Sommer S (2005) MHC class II DRB variability and parasite load in the striped mouse (Rhabdomys pumilio) in the southern Kalahari. Mol Biol Evol 22:1254–1259CrossRefPubMedGoogle Scholar
  21. Gordon HM, Whitlock HV (1939) A new technique for counting nematode eggs in sheep feaces. J Counc Sci Ind Res Melbourne 12:50–52Google Scholar
  22. Goüy de Bellocq J, Charbonnel N, Morand S (2008) Coevolutionary relationship between helminth diversity and MHC class II polymorphism in rodents. J Evol Biol 21:1144–1150CrossRefPubMedGoogle Scholar
  23. Harf R, Sommer S (2005) Association between MHC class II DRB alleles and parasite load in the hairy-footed gerbil, Gerbillurus paeba, in the southern Kalahari. Mol Ecol 14:85–91CrossRefPubMedGoogle Scholar
  24. Hedrick PW (1994) Evolutionary genetics of the major histocompatibility complex. Am Nat 143:945–964CrossRefGoogle Scholar
  25. Hedrick PW (2002) Pathogen resistance and genetic variation at MHC loci. Evolution 56:1902–1908PubMedGoogle Scholar
  26. Hedrick PW, Parker KM, Miller EL, Miller PS (1999) Major histocompatibility complex variation in the endangered Przewalski’s Horse. Genetics 152:1701–1710PubMedGoogle Scholar
  27. Holland O, Cowan P, Gleeson D, Chamley L (2008a) High variability in the MHC class II DA beta chain of the brushtail possum (Trichosurus vulpecula). Immunogenetics 60:775–781CrossRefPubMedGoogle Scholar
  28. Holland O, Cowan P, Gleeson D, Chamley L (2008b) Novel alleles in classical major histocompatibility complex class II loci of the brushtail possum (Trichosurus vulpecula). Immunogenetics 60:449–460CrossRefPubMedGoogle Scholar
  29. Hughes AL, Yeager M (1998) Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet 32:415–434CrossRefPubMedGoogle Scholar
  30. Klein J (1986) Natural history of the major histocompatibility complex. Wiley & Sons, New YorkGoogle Scholar
  31. Klein J, Horejsi V (1997) Immunology. Blackwell Science, OxfordGoogle Scholar
  32. Kurtz J, Kalbe M, Aeschlimann PB, Häberli MA, Wegner KM, Reusch TBH, Milinski M (2004) Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc R Soc Lond B Biol Sci 271:197–204CrossRefGoogle Scholar
  33. Lam MK-P, Belova K, Harrison GA, Coopera D (2001) Cloning of the MHC class II DRB cDNA from the brushtail possum (Trichosurus vulpecula). Immunol Lett 76:31–36CrossRefPubMedGoogle Scholar
  34. Langefors Å, Lohm J, Grahn M, Andersen Ø, von Schantz T (2001) Association between major histocompatibility complex class IIB alleles and resistance to Aeromonas salmonica in Atlantic salmon. Proc R Soc Lond B Biol Sci 268:479–485CrossRefGoogle Scholar
  35. Liersch S, Schmid-Hempel P (1998) Genetic variation within social insect colonies reduces parasite load. P Roy Soc Lond B Biol Sci 265:221-225CrossRefGoogle Scholar
  36. Lohm J, Grahn M, Langefors Å, Anderson Ø, Storset A, von Schantz T (2002) Experimental evidence for major histocompatibility complex-allele-specific resistance to a bacterial infection. Proc R Soc Lond B Biol Sci 269:2029–2033CrossRefGoogle Scholar
  37. Lorini ML, Oliveira JA, Persson VG (1994) Annual age structure and reproductive patterns in Marmosa incana (Lund, 1841) (Didelphidae, Marsupialia). Mamm Biol 59:65–73Google Scholar
  38. Mainguy J, Worley K, Côté S, Coltman D (2007) Low MHC DRB class II diversity in the mountain goat: past bottlenecks and possible role of pathogens and parasites. Conserv Genet 8:885–891CrossRefGoogle Scholar
  39. Martins EG, Bonato V (2004) On the diet of Gracilinanus microtarsus (Marsupialia, Didelphidae) in an Atlantic Rainforest fragment in south-eastern Brazil. Mamm Biol 69:58–60CrossRefGoogle Scholar
  40. Martins EG, Bonato V, da Silva CQ, dos Reis SF (2006) Partial semelparity in the neotropical didelphid marsupial Gracilinanus microtarsus. J Mammal 87:915–920CrossRefGoogle Scholar
  41. McCallum H, Dobson A (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol Evol 10:190–194CrossRefGoogle Scholar
  42. McKenzie LM, Cooper DW (1994) Low MHC class II variability in a marsupial. Reprod Fertil Dev 6:721–726CrossRefPubMedGoogle Scholar
  43. Meagher S (1999) Genetic diversity and Capillaria hepatica (Nematoda) prevalence in Michigan deer mouse populations. Evolution 53:1318–1324CrossRefGoogle Scholar
  44. Meyer-Lucht Y, Sommer S (2005) MHC diversity and the association to nematode parasitism in the yellow-necked mouse (Apodemus flavicollis). Mol Ecol 14:2233–2243CrossRefPubMedGoogle Scholar
  45. Meyer-Lucht Y, Otten C, Püttker T, Sommer S (2008) Selection, diversity and evolutionary patterns of the MHC class II DAB in free-ranging Neotropical marsupials. BMC Genet 9:39CrossRefPubMedGoogle Scholar
  46. Mikko S, Anderson L (1995) Low major histocompatibility complex class II diversity in European and North American moose. Proc Natl Acad Sci USA 92:4259–4263CrossRefPubMedGoogle Scholar
  47. Murchison EP, Tovar C, Hsu A et al (2010) The Tasmanian devil transcriptome reveals Schwann cell origins of a clonally transmissible cancer. Science 327:84–87CrossRefPubMedGoogle Scholar
  48. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefPubMedGoogle Scholar
  49. Nunn CL, Altizer S, Jones KE, Sechrest W (2003) Comparative tests of parasite species richness in primates. Am Nat 162:597–614CrossRefPubMedGoogle Scholar
  50. O’Brien SJ, Yuhki N (1999) Comparative genome organization of the major histocompatibility complex: lessons from the Felidae. Immunol Rev 167:133–144CrossRefPubMedGoogle Scholar
  51. O’Brien SJ, Roelke ME, Marker L, Newman A, Winkler CA, Meltzer D, Colly L, Evermann JF, Bush M, Wildt DE (1985) Genetic basis for species vulnerability in the cheetah. Science 227:1428–1434CrossRefPubMedGoogle Scholar
  52. Pardini R, Marques de Souza S, Braga-Neto R, Metzger JP (2005) The role of forest structure, fragment size and corridors in maintaining small mammal abundance and diversity in an Atlantic forest landscape. Biol Conserv 124:253–266CrossRefGoogle Scholar
  53. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatibility complex. Heredity 96:7–21PubMedGoogle Scholar
  54. Poulin R (1996) Sexual inequalities in helminth infections: a cost of being a male? Am Nat 147:287CrossRefGoogle Scholar
  55. Prugnolle F, Manica A, Charpentier M, Guégan JF, Guernier V, Balloux F (2005) Pathogen-driven selection and worldwide HLA class I diversity. Curr Biol 15:1022–1027CrossRefPubMedGoogle Scholar
  56. Püttker T, Meyer-Lucht Y, Sommer S (2006) Movement distances of five rodent and two marsupial species in forest fragments of the coastal Atlantic rainforest, Brazil. Ecotropica 12:131–139Google Scholar
  57. Püttker T, Pardini R, Meyer-Lucht Y, Sommer S (2008) Responses of five small mammal species to micro-scale variations in vegetation structure in secondary Atlantic forest remnants, Brazil. BMC Ecol 8:9CrossRefPubMedGoogle Scholar
  58. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  59. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni F, Hirota M (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153CrossRefGoogle Scholar
  60. Sandberg M, Eriksson L, Jonsson J, Sjostrom M, Wold S (1998) New chemical descriptors relevant for the design of biologically active peptides. A multivariate characterization of 87 amino acids. J Med Chem 41:2481–2491CrossRefPubMedGoogle Scholar
  61. Schad J, Sommer S, Ganzhorn J (2004) MHC variability of a small lemur in the littoral forest fragments of south-eastern Madagascar. Conserv Genet 5:299–309CrossRefGoogle Scholar
  62. Schad J, Ganzhorn JU, Sommer S (2005) MHC constitution and parasite burden in the Malagasy mouse lemur, Microcebus murinus. Evolution 59:439–450PubMedGoogle Scholar
  63. Schneider S, Vincek V, Tichy H, Figueroa F, Klein J (1991) MHC class II genes of a marsupial, the red-necked wallaby (Macropus rufogriseus): identification of new gene families. Mol Biol Evol 8:753–766PubMedGoogle Scholar
  64. Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163CrossRefGoogle Scholar
  65. Schwaiger FW, Gostomski D, Stear MJ (1995) An ovine major histocompatibility complex DRB1 allele is associated with low fecal counts following natural, predominantly Ostertagia circumcincta infection. Int J Parasitol 25:815–822CrossRefPubMedGoogle Scholar
  66. Schwensow N, Fietz J, Dausmann K, Sommer S (2007) Neutral versus adaptive genetic variation in parasite resistance: importance of MHC-supertypes in a free-ranging primate. Heredity 99:265–277CrossRefPubMedGoogle Scholar
  67. Seivwright LJ, Redpath SM, Mougeot F, Watt L, Hudson PJ (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J Helminthol 78:69–76CrossRefPubMedGoogle Scholar
  68. Sette A, Sidney J (1999) Nine major HLA class I supertypes account for the vast preponderance of HLA-A and -B polymorphism. Immunogenetics 50:201–212CrossRefPubMedGoogle Scholar
  69. Siddle H, Kreiss A, Eldridge MDB, Noonan E, Clarke CJ, Pyecroft S, Woods GM, Belov K (2007a) From the cover: transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc Natl Acad Sci USA 104:16221–16226CrossRefPubMedGoogle Scholar
  70. Siddle H, Sanderson C, Belov K (2007b) Characterization of major histocompatibility complex class I and class II genes from the Tasmanian devil (Sarcophilus harrisii). Immunogenetics 59:753–760CrossRefPubMedGoogle Scholar
  71. Slade RW, McCallum HI (1992) Overdominant vs frequency-dependent selection at MHC loci. Genetics 132:861–862PubMedGoogle Scholar
  72. Sommer S (2003) Effects of habitat fragmentation and changes of dispersal behaviour after a recent population decline on the genetic variability of noncoding and coding DNA of a monogamous Malagasy rodent. Mol Ecol 12:2845–2851CrossRefPubMedGoogle Scholar
  73. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Front Zool 2:16CrossRefPubMedGoogle Scholar
  74. SOS Mata Atlântica and Instituto Nacional de Pesquisas Espaciais (2008) Atlas dos remanescentes florestais da Mata Atlântica, período de 2000 a 2005Google Scholar
  75. Soulsby EJL (1982) Helminths, arthropods and protozoa of domesticated animals, Lea & Febiger, PhiladelphiaGoogle Scholar
  76. Southwood S, Sidney J, Kondo A, del Guercio M-F, Appella E, Hoffman S, Kubo RT, Chesnut RW, Grey HM, Sette A (1998) Several common HLA-DR types share largely overlapping peptide binding repertoires. J Immunol 160:3363–3373PubMedGoogle Scholar
  77. Spielman D, Brook B, Briscoe D, Frankham R (2004) Does inbreeding and loss of genetic diversity decrease disease resistance? Conserv Genet 5:439–448CrossRefGoogle Scholar
  78. Stear MJ, Bishop SC, Doligalska M, Duncan JL, Holmes PH, Irvine J, McCririe L, McKellar QA, Sinski E, Murray M (1995) Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunol 17:643–652CrossRefPubMedGoogle Scholar
  79. Stear MJ, Bairden K, Duncan JL, Holmes PH, McKellar QA, Park M, Strain S, Murray M, Bishop SC, Gettinby G (1997) How hosts control worms. Nature 389:27CrossRefPubMedGoogle Scholar
  80. Stone W, Bruun D, Manis G, Holste S, Hoffman E, Spong K, Walunas T (1996) The immunobiology of the marsupial, Monodelphis domestica. In: Stolen J, Fletcher T, Bayne C, Secombes C, Zelikoff J, Twerdok L, Anderson D (eds) Modulators of immune responses: the evolutionary trail. SOS Publications, Fair Haven, NJ, pp 149–165Google Scholar
  81. Stone W, Brunn D, Foster E, Manis G, Hoffman E, Saphire D, VandeBerg J, Infante A (1998) Absence of a significant mixed lymphocyte reaction in a marsupial (Monodelphis domestica). Lab Anim Sci 48:184–189PubMedGoogle Scholar
  82. Stone W, Bruun D, Fuqua C, Glass L, Reeves A, Holste S, Figueroa F (1999) Identification and sequence analysis of an Mhc class II B gene in a marsupial (Monodelphis domestica). Immunogenetics 49:461–463CrossRefPubMedGoogle Scholar
  83. Tabarelli M, Cardoso da Silva J, Gascon C (2004) Forest fragmentation, synergisms and the impoverishment of neotropical forests. Biodivers Conserv 13:1419–1425CrossRefGoogle Scholar
  84. Tabarelli M, Pinto LP, Silva JMC, Hirota M, Bede L (2005) Challenges and opportunities for biodiversity conservation in the Brazilian Atlantic forest. Conserv Biol 19:695–700CrossRefGoogle Scholar
  85. Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124:967–978PubMedGoogle Scholar
  86. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  87. Teixeira AMG, Soares-Filho BS, Freitas SR, Metzger JP (2009) Modeling landscape dynamics in an Atlantic Rainforest region: implications for conservation. Forest Ecol Manag 257:1219–1230CrossRefGoogle Scholar
  88. Trachtenberg E, Korber B, Sollars C, Kepler TB, Hraber PT, Hayes E, Funkhouser R, Fugate M, Theiler J, Hsu YS, Kunstman K, Wu S, Phair J, Erlich H, Wolinsky S (2003) Advantage of rare HLA supertype in HIV disease progression. Nat Med 9:928–935CrossRefPubMedGoogle Scholar
  89. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027CrossRefPubMedGoogle Scholar
  90. Umetsu F, Pardini R (2007) Small mammals in a mosaic of forest remnants and anthropogenic habitats-evaluating matrix quality in an Atlantic forest landscape. Landsc Ecol 22:517–530CrossRefGoogle Scholar
  91. Vieira EM, Monteiro-Filho ELA (2003) Vertical stratification of small mammals in the Atlantic Rainforest of south-eastern Brazil. J Trop Ecol 19:501–507CrossRefGoogle Scholar
  92. Wan Q-H, Zhu L, Wu HUA, Fang S-G (2006) Major histocompatibility complex class II variation in the giant panda (Ailuropoda melanoleuca). Mol Ecol 15:2441–2450CrossRefPubMedGoogle Scholar
  93. Wegner KM, Kalbe M, Kurtz J, Reusch TBH, Milinski M (2003a) Parasite selection for immunogenetic optimality. Science 301:1343CrossRefPubMedGoogle Scholar
  94. Wegner KM, Reusch TBH, Kalbe M (2003b) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol 16:224–232CrossRefPubMedGoogle Scholar
  95. Westerdahl H, Waldenström J, Hansson B, Hasselquist D, von Schantz T, Bensch S (2005) Associations between malaria and MHC genes in a migratory songbird. Proc R Soc Lond B Biol Sci 272:1511–1518CrossRefGoogle Scholar
  96. Woodroffe R (1999) Managing disease threats to wild mammals. Anim Conserv 2:185–193CrossRefGoogle Scholar
  97. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556PubMedGoogle Scholar
  98. Yuhki N, O’Brien SJ (1990) DNA variation of the mammalian major histocompatibility complex reflects genomic diversity and population history. Proc Natl Acad Sci USA 87:836–840CrossRefPubMedGoogle Scholar
  99. Zuk M (1990) Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitol Today 6:231–233CrossRefPubMedGoogle Scholar
  100. Zuk M, McKean KA (1996) Sex differences in parasite infections: Patterns and processes. Int J Parasitol 26:1009–1024CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Yvonne Meyer-Lucht
    • 1
  • Celine Otten
    • 1
  • Thomas Püttker
    • 1
  • Renata Pardini
    • 2
  • Jean Paul Metzger
    • 3
  • Simone Sommer
    • 1
  1. 1.Leibniz Institute for Zoo and Wildlife ResearchEvolutionary GeneticsBerlinGermany
  2. 2.Departamento de Zoologia, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil
  3. 3.Laboratório de Ecologia de Paisagem e Conservação (LEPaC), Departamento de Ecologia, Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil

Personalised recommendations