Host sexual dimorphism and parasite adaptation

PLoS Biology

Volumn 10, Issue 2, 2012, Pages

  Duneau, David ^a,b   Ebert, Dieter ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE BEHAVIOR; ANIMAL BEHAVIOR; ARTICLE; ENVIRONMENT; GENOTYPE; NONHUMAN; PARASITE; PARASITE ISOLATION; PARASITE TRANSMISSION; PARASITE VIRULENCE; PHENOTYPE; POPULATION STRUCTURE; SEX DIFFERENCE; SOCIAL BEHAVIOR; ADAPTATION; ANIMAL; DISEASE TRANSMISSION; EVOLUTION; FEMALE; HOST PARASITE INTERACTION; HUMAN; MALE; PARASITOLOGY; PARASITOSIS; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; HOST-PARASITE INTERACTIONS; HUMANS; MALE; PARASITES; PARASITIC DISEASES; SEX CHARACTERISTICS; SEX FACTORS;

EID: 84857482777     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001271     Document Type: Article

References (98)

1. Zuk M, McKean K. A, (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26: 1009-1023.
2. Dhangadamajhi G, Kar S. K, Ranjit M. R, (2009) High prevalence and gender bias in distribution of Plasmodium malariae infection in central east-coast India. Trop Biomed 26: 326-333.
3. Abu-Madi M. A, Behnke J. M, Prabhaker K. S, Al-Ibrahim R, Lewis J. W, (2010) Intestinal helminths of feral cat populations from urban and suburban districts of Qatar. Vet Parasitol 168: 284-292.
4. Deviche P, Fokidis H. B, Lerbour B, Greiner E, (2010) Blood parasitaemia in a high latitude flexible breeder, the white-winged crossbill, Loxia leucoptera: contribution of seasonal relapse versus new inoculations. Parasitology 137: 261-273.
5. Locklin J. L, Vodopich D. S, (2010) Patterns of gregarine parasitism in dragonflies: host, habitat, and seasonality. Parasitol Res 107: 75-87.
6. Folstad I, Karter A. J, (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139: 603-622.
7. Stoehr A. M, Kokko H, (2006) Sexual dimorphism in immunocompetence: what does life-history theory predict? Behav Ecol 17: 751-756.
8. McKean K. A, Nunney L, (2005) Bateman's principle and immunity: phenotypically plastic reproductive strategies predict changes in immunological sex differences. Evolution 59: 1510-1517.
9. Rolff J, (2002) Bateman's principle and immunity. Proc Biol Sci 269: 867-872.
10. Zuk M, Stoehr A. M, (2010) Sex differences in susceptibility to infection: an evolutionary perspective. In: Klein S. L, Robert C. W, editors. Sex hormones and immunity to infection Berlin Springer.
11. Schmid-Hempel P, (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics Oxford Oxford University Press.
12. Lively C. M, (1989) Adaptation by a parasitic trematode to local-populations of its snail host. Evolution 43: 1663-1671.
13. Williams G. C, (1966) Adaptation and natural selection Princeton Princeton University Press.
14. Kawecki T. J, Ebert D, (2004) Conceptual issues in local adaptation. Ecol Lett 7: 1225-1241.
15. Beldade P, Mateus A. R, Keller R. A, (2011) Evolution and molecular mechanisms of adaptive developmental plasticity. Mol Ecol 20: 1347-1363.
16. Scheiner S. M, (1993) Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Syst 24: 35-68.
17. West S. A, (2009) Sex allocation Princeton Princeton University Press.
18. Hardy I. C. W, (2002) Sex ratios: concepts and research methods Cambridge Cambridge University Press.
19. Hamilton W. D, (1967) Extraordinary sex-ratio. Science 156: 477-488.
20. Clutton-Brock T. H, Iason G. R, (1986) Sex ratio variation in mammals. Q Rev Biol 61: 339-374.
21. Allsop D. J, West S. A, (2004) Sex-ratio evolution in sex changing animals. Evolution 58: 1019-1027.
22. Otterstatter M. C, Whidden T. L, (2004) Patterns of parasitism by tracheal mites (Locustacarus buchneri) in natural bumble bee populations. Apidologie 35: 351-357.
23. Werren J. H, Windsor D. M, (2000) Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc Biol Sci 267: 1277-1285.
24. Laursen L, Bekof M, (1978) Loxodonta africana. Mammalian Species 92: 8.
25. Main M. B, Weckerly F. W, Vernon C. B, (1996) Sexual segregation in Ungulates: new directions for research. J Mammal 77: 449-461.
26. Meagher M, (1986) Bison bison. Mammalian Species 226: 1-8.
27. Ferrari N, Rosa R, Lanfranchi P, Ruckstuhl K. E, (2010) Effect of sexual segregation on host-parasite interaction: model simulation for abomasal parasite dynamics in alpine ibex (Capra ibex). Int J Parasitol 40: 1285-1293.
28. Moore S. L, Wilson K, (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297: 2015-2018.
29. Amadon D, (1959) The significance of sexual differences in size among birds. Proc Am Philos Soc 103: 531-536.
30. Teder T, Tammaru T, (2005) Sexual size dimorphism within species increases with body size in insects. Oikos 108: 321-334.
31. Vollrath F, (1998) Dwarf males. Trends Ecol Evol 13: 159-163.
32. Darwin C, (1851) A monograph of the sub-class Cirripedia, with figures of all the species. Vol I: The Lepadidae London The Ray Society.
33. Baker D. G, (1998) Natural pathogens of laboratory mice, rats, and rabbits and their effects on research. Clin Microbiol Rev 11: 231-266.
34. Litvinova E. A, Goncharova E. P, Zaydman A. M, Zenkova M. A, Moshkin M. P, (2010) Female scent signals enhance the resistance of male mice to influenza. PLoS ONE 5: e9473 doi:10.1371/journal.pone.0009473.
35. Bendinelli M, Pistello M, Lombardi S, Poli A, Garzelli C, et al. (1995) Feline immunodeficiency virus: an interesting model for AIDS studies and an important cat pathogen. Clin Microbiol Rev 8: 87-112.
36. Robinson S. A, Forbes M. R, Hebert C. E, McLauglin J. D, (2010) Male biased parasitism in cormorants and relationships with foraging ecology on lake Erie, Canada. Waterbirds 33: 307-313.
37. Boinski S, (1988) Sex-differences in the foraging behavior of squirrel monkeys in a seasonal habitat. Behav Ecol Sociobiol 23: 177-186.
38. Weimerskirch H, Shaffer S. A, Tremblay Y, Costa D. P, Gadenne H, et al. (2009) Species and sex-specific differences in foraging behaviour and foraging zones in blue-footed and brown boobies in the Gulf of California. Mar Ecol Prog Ser 391: 267-278.
39. Whitfield J. T, Pako W. H, Collinge J, Alpers M. P, (2008) Mortuary rites of the South Fore and kuru. Philos Trans R Soc Lond B Biol Sci 363: 3721-3724.
40. Post D. M, Armbrust T. S, Horne E. A, Goheen J. R, (2001) Sexual segregation results in differences in content and quality of Bison (Bos bison) diets. J Mammal 82: 407-413.
41. Fragaszy D. M, Boinski S, (1995) Patterns of individual diet choice and efficiency of foraging in wedge-capped capucin monkey (Cebus olivaceus). J Comp Psychol 109: 339-348.
42. Greenwood P. J, (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28: 1140-1162.
43. Klein S. L, (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26: 247-264.
44. Beagley K. W, Gockel C. M, (2003) Regulation of innate and adaptive immunity by the female sex hormones oestradiol and progesterone. FEMS Immunol Med Microbiol 38: 13-22.
45. Grossman C. J, (1985) Interactions between the gonadal steroids and the immune system. Science 227: 257-261.
46. Yao G. H, Liang J, Han X. D, Hou Y. Y, (2003) In vivo modulation of the circulating lymphocyte subsets and monocytes by androgen. Int Immunopharmacol 3: 1853-1860.
47. Rettew J. A, Huet-Hudson Y. M, Marriott I, (2008) Testosterone reduces macrophage expression in the mouse of toll-like receptor 4, a trigger for inflammation and innate immunity. Biol Reprod 78: 432-437.
48. Cox R. M, John-Alder H. B, (2007) Increased mite parasitism as a cost of testosterone in male striped plateau lizards Sceloporus virgatus. Functional Ecology 21: 327-334.
49. Swearer S. E, Robertson D. R, (1999) Life history, pathology, and description of Kudoa ovivora n. sp (Myxozoa, Myxosporea): an ovarian parasite of Caribbean labroid fishes. J Parasitol 85: 337-353.
50. Sitja-Bobadilla A, Alvarez-Pellitero P, (1990) Sphaerospora testicularis sp. nov. (Myxosporea: Sphaerosporidae) in wild and cultured sea bass, Dicentrarchus labrax (L.), from the Spanish Mediterranean area. J Fish Dis 13: 193-203.
51. Edmunds G. F, Alstad D. N, (1978) Coevolution in insect herbivores and conifers. Science 199: 941-945.
52. Greischar M. A, Koskella B, (2007) A synthesis of experimental work on parasite local adaptation. Ecol Lett 10: 418-434.
53. Scharer L, Vizoso D. B, (2003) Earlier sex change in infected individuals of the protogynous reef fish Thalassoma bifasciatum. Behav Ecol Sociobiol 55: 137-143.
54. Rice W. R, Chippindale A. K, (2002) The evolution of hybrid infertility: perpetual coevolution between gender-specific and sexually antagonistic genes. Genetica 116: 179-188.
55. Bonduriansky R, Chenoweth S. F, (2009) Intralocus sexual conflict. Trends Ecol Evol 24: 280-288.
56. Sherman L. A, Temple R, Merkatz R. B, (1995) Women in clinical trials: an FDA perspective. Science 269: 793-795.
57. Kim A. M, Tingen C. M, Woodruff T. K, (2010) Sex bias in trials and treatment must end. Nature 465: 688-689.
58. Baylis F, (2010) Pregnant women deserve better. Nature 465: 689-690.
59. Zucker I, Beery A. K, (2010) Males still dominate animal studies. Nature 465: 690-690.
60. Meinert C. L, (1995) The inclusion of women in clinical trials. Science 269: 795-796.
61. Cook I. F, (2008) Sexual dimorphism of humoral immunity with human vaccines. Vaccine 26: 3551-3555.
62. Pfister M, Kursteiner O, Hilfiker H, Favre D, Durrer P, et al. (2005) Immunogenicity and safety of BERNA-YF compared with two other 17D yellow fever vaccines in a phase 3 clinical trial. Am J Trop Med Hyg 72: 339-346.
63. Ferrari N, Cattadori I. M, Nespereira J, Rizzoli A, Hudson P. J, (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Lett 7: 88-94.
64. Luong L. T, Grear D. A, Hudson P. J, (2009) Male hosts are responsible for the transmission of a trophically transmitted parasite, Pterygodermatites peromysci, to the intermediate host in the absence of sex-biased infection. Int J Parasitol 39: 1263-1268.
65. Hawkins B. A, Thomas M. B, Hochberg M. E, (1993) Refuge theory and biological control. Science 262: 1429-1432.
66. Altermatt F, Ebert D, (2008) Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecol Lett 11: 918-928.
67. Ganz H. H, Ebert D, (2010) Benefits of host genetic diversity for resistance to infection depend on parasite diversity. Ecology 91: 1263-1268.
68. Fierer N, Hamady M, Lauber C. L, Knight R, (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci U S A 105: 17994-17999.
69. Kaciuba-Uscilko H, Grucza R, (2001) Gender differences in thermoregulation. Curr Opin Clin Nutr Metab Care 4: 533-536.
70. Pilgrim E. M, Pitts J. P, (2006) A molecular method for associating the dimorphic sexes of velvet ants (Hymenoptera: Mutillidae). J Kans Entomol Soc 79: 222-230.
71. Tinsley R. C, (1989) The effects of host sex on transmission success. Parasitol Today 5: 190-195.
72. Bouwman K. M, Hawley D. M, (2010) Sickness behaviour acting as an evolutionary trap? Male house finches preferentially feed near diseased conspecifics. Biol Lett 6: 462-465.
73. O'Donnell S, Beshers S. N, (2004) The role of male disease susceptibility in the evolution of haplodiploid insect societies. Proc Biol Sci 271: 979-983.
74. Boomsma J. J, Baer B, Heinze J, (2005) The evolution of male traits in social insects. Annu Rev Entomol 50: 395-420.
75. Lee A. K, Cockburn A, (1985) Evolutionary ecology of marsupials Cambridge Cambridge University Press.
76. Anderson D. L, (2000) Variation in the parasitic bee mite Varroa jacobsoni Oud. Apidologie 31: 281-292.
77. Boot W. J, Tan N. Q, Dien P. C, Huan L. V, Dung N. V, et al. (1997) Reproductive success of Varroa jacobsoni in brood of its original host, Apis cerana, in comparison to that of its new host, A. mellifera (Hymenoptera: Apidae). Bull Entomol Res 87: 119-126.
78. Leconte Y, Arnold G, Trouiller J, Masson C, Chappe B, et al. (1989) Attraction of the parasitic mite Varroa to the drone larvae of honey bees by simple aliphatic esters. Science 245: 638-639.
79. Caillaud D, Prugnolle F, Durand P, Theron A, de Meeus T, (2006) Host sex and parasite genetic diversity. Microbes Infect 8: 2477-2483.
80. van Harmelen J, Wood R, Lambrick M, Rybicki E. P, Williamson A-L, et al. (1997) An association between HIV-1 subtypes and mode of transmission in Cape Town, South Africa. AIDS 11: 81-87.
81. Whipps C. M, Kent M. L, (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J Eukaryot Microbiol 53: 364-373.
82. Christe P, Glaizot O, Evanno G, Bruyndonckx N, Devevey G, et al. (2007) Host sex and ectoparasites choice: preference for, and higher survival on female hosts. J Anim Ecol 76: 703-710.
83. Mikheev V. N, Pasternak A. F, Valtonen E. T, (2004) Tuning host specificity during the ontogeny of a fish ectoparasite: behavioural responses to host-induced cues. Parasitol Res 92: 220-224.
84. Osterkamp J, Wahl U, Schmalfuss G, Haas W, (1999) Host-odour recognition in two tick species is coded in a blend of vertebrate volatiles. J Comp Physiol A 185: 59-67.
85. Krasnov B. R, Khokhlova I. S, Oguzoglu I, Burdelova N. V, (2002) Host discrimination by two desert fleas using an odour cue. Anim Behav 64: 33-40.
86. Rae R. G, Robertson J. F, Wilson M. J, (2009) Chemoattraction and host preference of the gastropod parasitic nematod Phasmarhabditis hermaphrodita. J Parasitol 95: 517-526.
87. Hassan A. H. M, Haberl B, Hertel J, Haas W, (2003) Miracidia of an Egyptian strain of Schistosoma mansoni differentiate between sympatric snail species. J Parasitol 89: 1248-1250.
88. Allan R, Rollinson D, Smith J. E, Dunn A. M, (2009) Host choice and penetration by Schistosoma haematobium miracidia. J Helminthol 83: 33-38.
89. Christe P, Giorgi M. S, Vogel P, Arlettaz R, (2003) Differential species-specific ectoparasitic mite intensities in two intimately coexisting sibling bat species: resource-mediated host attractiveness or parasite specialization? J Anim Ecol 72: 866-872.
90. Rosenkranz P, Aumeier P, Ziegelmann B, (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103: S96-S119.
91. Rath W, (1999) Co-adaptation of Apis cerana Fabr. and Varroa jacobsoni Oud. Apidologie 30: 97-110.
92. Nazzi F, Bortolomeazzi R, Della Vedova G, Del Piccolo F, Annoscia D, et al. (2009) Octanoic acid confers to royal jelly varroa-repellent properties. Naturwissenschaften 96: 309-314.
93. Calderone N. W, Kuenen L. P. S, (2003) Differential tending of worker and drone larvae of the honey bee, Apis mellifera, during the 60 hours prior to cell capping. Apidologie 34: 543-552.
94. Boot W. J, Schoenmaker J, Calis J. N. M, Beetsma J, (1995) Invasion of Varroa jacobsoni into drone brood cells of the honey bee, Apis mellifera. Apidologie 26: 109-118.
95. Hoeg J. T, (1995) The biology and the life-cycle of the rhizocephala (Cirripedia). J Mar Biol Assoc UK 75: 517-550.
96. Fisher F. M, (1963) Production of host endocrine substances by parasites. Ann N Y Acad Sci 113: 63-87.
97. Werren J. H, Baldo L, Clark M. E, (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741-751.
98. Dunn A. M, Terry R. S, Smith J. E, (2001) Transovarial transmission in the microsporidia. Adv Parasitol 48: 57-100.