Advertisement

Naturwissenschaften

, Volume 101, Issue 10, pp 839–849 | Cite as

A comparative study of an innate immune response in Lamprologine cichlid fishes

  • Constance M. O’ConnorEmail author
  • Adam R. Reddon
  • Susan E. Marsh-Rollo
  • Jennifer K. Hellmann
  • Isaac Y. Ligocki
  • Ian M. Hamilton
  • Sigal Balshine
Original Paper

Abstract

Social interactions facilitate pathogen transmission and increase virulence. Therefore, species that live in social groups are predicted to suffer a higher pathogen burden, to invest more heavily in immune defence against pathogens, or both. However, there are few empirical tests of whether social species indeed invest more heavily in immune defence than non-social species. In the current study, we conducted a phylogenetically controlled comparison of innate immune response in Lamprologine cichlid fishes. We focused on three species of highly social cichlids that live in permanent groups and exhibit cooperative breeding (Julidochromis ornatus, Neolamprologus pulcher and Neolamprologus savoryi) and three species of non-social cichlids that exhibit neither grouping nor cooperative behaviour (Telmatochromis temporalis, Neolamprologus tetracanthus and Neolamprologus modestus). We quantified the innate immune response by injecting wild fishes with phytohaemagglutinin (PHA), a lectin that causes a cell-mediated immune response. We predicted that the three highly social species would show a greater immune reaction to the PHA treatment, indicating higher investment in immune defence against parasites relative to the three non-social species. We found significant species-level variation in immune response, but contrary to our prediction, this variation did not correspond to social system. However, we found that immune response was correlated with territory size across the six species. Our results indicate that the common assumption of a positive relationship between social system and investment in immune function may be overly simplistic. We suggest that factors such as rates of both in-group and out-group social interactions are likely to be important mediators of the relationship between sociality and immune function.

Keywords

Sociality Group living Cooperation Inflammatory response Parasite Pathogen Phytohaemagglutinin Teleost Lake Tanganyika 

Notes

Acknowledgments

The authors wish to thank Danny Sinyinza, Harris Phiri, Partrick Ngalande and Clement Sichamba at the Zambian Department of Fisheries, Dr. Cyprian Katongo at the University of Zambia in Lusaka, Peter Sekazway from Kasakalawe Village and Augustine Mwewa, Celestine Mwewa, Fernandez Mwewa, Gegwin Kapembwe, Damius Kapembwe and the rest of the wonderful staff at the Tanganyika Science Lodge for logistical support. The research was supported by a Natural Sciences and Engineering Research Council of Canada Discovery (NSERC) grant and equipment grant to SB as well as Ontario Innovation Trust and Canadian Foundation for Innovation awards to SB. Further funding for the field research was provided by a Journal of Experimental Biology Travelling Fellowship to CMO and research grants to ARR from the Canadian Society of Zoologists and McMaster School of Graduate Studies. CMO received support from an E.B. Eastburn Postdoctoral Fellowship from the Hamilton Community Foundation, and is currently supported by an NSERC Postdoctoral Fellowship. ARR received support from the Margo Wilson and Martin Daly Ontario Graduate Scholarship and is currently supported by the Richard H. Tomlinson Postdoctoral Fellowship and an NSERC Postdoctoral Fellowship. IYL and JKH are supported by the Department of Evolution, Ecology and Organismal Biology at The Ohio State University, The Ohio State University Fish Systematics Endowment, and the SciFund Challenge. JKH is supported by the American Academy of Underwater Sciences. SB is supported by the Canada Research Chair Program and the NSERC Discovery Program.

References

  1. Agnew P, Koella JC (1999) Life history interactions with environmental conditions in a host-parasite relationship and the parasite’s mode of transmission. Evol Ecol 13:67–89Google Scholar
  2. Alexander RD (1974) The evolution of social behaviour. Annu Rev Ecol Syst 5:325–383Google Scholar
  3. Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics AP, Cunningham AA, Dobon AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC (2003) Social organization and parasite risk in mammals: Integrating theory and empirical studies. Ann Rev Ecol Evol Syst 34:517–547Google Scholar
  4. Anderson RM, May RM (1979) Population biology of infectious diseases: part I. Nature 280:361–367PubMedGoogle Scholar
  5. Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85:411–426PubMedGoogle Scholar
  6. Ardia DR, Clotfelter ED (2006) The novel application of an immunological technique reveals the immunosuppressive effect of phytoestrogens in Betta splendens. J Fish Biol 68:144–149Google Scholar
  7. Awata S, Munehara H, Kohda M (2005) Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses. Behav Ecol Sociobiol 58:506–516Google Scholar
  8. Balshine S, Leach B, Neat F, Reid H, Taborsky M, Werner N (2001) Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). Behav Ecol Sociobiol 50:134–140Google Scholar
  9. Balshine-Earn S, Neat FC, Reid H, Taborsky M (1998) Paying to stay or paying to breed? Field evidence for direct benefits of helping in a cooperatively breeding fish. Behav Ecol 9:432–438Google Scholar
  10. Bergmüller R, Heg D, Peer K, Taborksy M (2005) Extended safe havens and between-group dispersal of helpers in a cooperatively breeding cichlid. Behaviour 142:1643–1667Google Scholar
  11. Bergmüller R, Johnstone R, Russell A, Bshary R (2007) Integrating cooperative breeding into theoretical concepts of cooperation. Behav Process 76:61–72Google Scholar
  12. Bordes F, Blumstein DT, Morand S (2007) Rodent sociality and parasite diversity. Biol Lett 3:692–694PubMedCentralPubMedGoogle Scholar
  13. Brichard P (1989) Cichlids and all the other fishes of Lake Tanganyika. THF Publications, Neptune CityGoogle Scholar
  14. Brown CR (1986) Cliff swallow colonies as information-centers. Science 234:83–85PubMedGoogle Scholar
  15. Brown CR, Brown MB (1986) Ectoparasitism as a cost of coloniality in cliff swallows (Hirundo pyrrhonota). Ecology 67:1206–1218Google Scholar
  16. Bukinga FM, Vanhove MPM, Steenberge MV, Pariselle A (2012) Ancyrocephalidae (Monogenea) of Lake Tanganyika: III: Cichlidogyrus infecting the world’s biggest cichlid and the non-endemic tribes Haplochromini, Oreochromini and Tylochromini (Teleostei, Cichlidae). Parasitol Res 111:2049–2061Google Scholar
  17. Caspi RR, Rozenszajin LA, Gotheif Y, Pergamenikov-Litvak T, Avtalion RR (1982) The cells involved in the immune response of fish: II. PHA-induced clonal proliferation of carp lymphocytes in soft agar culture. Dev Comp Immunol 6:682–692Google Scholar
  18. Clayton DH, Tompkins DM (1994) Ectoparasite virulence is linked to mode of transmission. Proc R Soc Lond B 256:211–217Google Scholar
  19. Clotfelter ED, Ardia DR, McGraw KJ (2007) Red fish, blue fish: trade-offs between pigmentation and immunity in Betta splendens. Behav Ecol 18:1139–1145Google Scholar
  20. Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72PubMedGoogle Scholar
  21. Coté IM, Poulin R (1995) Parasitism and group-size in social animals—a meta-analysis. Behav Ecol 6:159–165Google Scholar
  22. Cresswell W (1994) Flocking is an effective anti-predation strategy in redshanks, Tringa totanus. Anim Behav 47:433–442Google Scholar
  23. Danchin E, Giraldeau L-A, Wagner RH (2008) Animal aggregations: hypotheses and controversies. In: Danchin E, Giraldeau L-A, Cezilly F (eds) Behavioural ecology. Oxford University Press, Oxford, pp 503–545Google Scholar
  24. Davies CR, Ayres JM, Dye C, Deane LM (1991) Malaria infection-rate of Amazonian primates increases with body-weight and group-size. Funct Ecol 5:655–662Google Scholar
  25. Day JJ, Santini S, Garcia-Moreno J (2007) Phylogenetic relationships of the Lake Tanganyika cichlid tribe Lamprologini: the story from mitochondrial DNA. Mol Phylogenet Evol 45:629–642PubMedGoogle Scholar
  26. Desjardins JK, Hazelden MR, Van der Kraak GJ, Balshine S (2006) Male and female cooperatively breeding fish provide support for the ‘challenge hypothesis’. Behav Ecol 17:149–154Google Scholar
  27. Diepeveen ET, Roth O, Salzburger W (2013) Immune-related functions of the Hivep gene family in East African cichlid fishes. G3: Genes Genomes Genet 3:2205–2217Google Scholar
  28. Dierkes P, Heg D, Taborsky M, Skubic E, Achmann R (2005) Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid. Ecol Lett 8:968–975Google Scholar
  29. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. http://beast.bio.ed.ac.uk/Main_Page
  30. Drummond AJ, Ho SY, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88PubMedCentralPubMedGoogle Scholar
  31. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUTi and the BEAST 1.7. Mol Biol Evol 29:1969–1973PubMedCentralPubMedGoogle Scholar
  32. Ebert D, Hamilton WD (1996) Sex against virulence: the coevolution of parasitic diseases. Trends Ecol Evol 11:A79–A82Google Scholar
  33. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. http://www.ebi.ac.uk/Tools/msa/muscle/
  34. Elgar MA (1989) Predator vigilance and group-size in mammals and birds: a critical review of the empirical evidence. Biol Rev Camb Philos Soc 64:13–33PubMedGoogle Scholar
  35. Ewald PW (1983) Host-parasite relations, vectors, and the evolution of disease severity. Annu Rev Ecol Syst 14:465–485Google Scholar
  36. Ewald PW (1987) Transmission modes and evolution of the parasitism-mutualism continuum. Ann N Y Acad Sci 503:295–306PubMedGoogle Scholar
  37. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15Google Scholar
  38. Fincher CL, Thornhill R (2012) Parasite-stress promotes in-group assortative sociality: the cases of strong family ties and heightened religiosity. Behav Brain Sci 35:61–79PubMedGoogle Scholar
  39. Fincher CL, Thornhill R, Murray DR, Schaller M (2008) Pathogen prevalence predicts human cross-cultural variability in individualism/collectivism. Proc R Soc Lond B 275:1279–1285Google Scholar
  40. Frank SA (1992) A kin selection model for the evolution of virulence. Proc R Soc Lond B 250:195–197Google Scholar
  41. Frank SA (1996) Models of parasite virulence. Q Rev Biol 71:37–78PubMedGoogle Scholar
  42. Games PA, Howell JF (1976) Pairwise multiple comparison procedures with unequal N’s and/or variances: a Monte Carlo study. J Educ Stat 1:113–125Google Scholar
  43. García-Longoria L, Garamszegi LZ, Møller AP (2014) Host escape behaviour and blood parasite infections in birds. Behav Ecol 29:2014. doi: 10.1093/beheco/aru066 Google Scholar
  44. Gaston A (1978) The evolution of group territorial behavior and cooperative breeding. Am Nat 112:1091–1100Google Scholar
  45. Gillardin C, Vanhove MPM, Pariselle A, Huyse T, Volckaert FAM (2011) Ancyrocephalidae (Monogenea) of Lake Tanganyika: II: description of the first Cichlidogyrus spp. Parasites from Tropheini fish hosts (Teleostei, Cichlidae). Parasitol Res 110:305–313PubMedGoogle Scholar
  46. Goodson JL, Evans AK (2004) Neural responses to territorial challenge and nonsocial stress in male song sparrows: segregation, integration, and modulation by a vasopressin V1 antagonist. Horm Behav 46:371–381PubMedGoogle Scholar
  47. Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311PubMedGoogle Scholar
  48. Hamilton WD, Axelrod R, Tanese R (1990) Sexual reproduction as an adaptation to resist parasites (a review). Proc Natl Acad Sci U S A 87:3566–3573PubMedCentralPubMedGoogle Scholar
  49. Harvey PH, Pagel M (1991) The comparative method in evolutionary biology. Oxford University Press, OxfordGoogle Scholar
  50. Hatchwell BJ (2009) The evolution of cooperative breeding in birds: kinship, dispersal and life history. Phil Trans R Soc B 364:3217–3227PubMedCentralPubMedGoogle Scholar
  51. Hatchwell B, Komdeur J (2000) Ecological constraints, life history traits and the evolution of cooperative breeding. Anim Behav 59:1079–1086PubMedGoogle Scholar
  52. Hau M (2007) Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. BioEssays 29:133–144PubMedGoogle Scholar
  53. Heg D, Bachar Z (2006) Cooperative breeding in the Lake Tanganyika cichlid Julidochromis ornatus. Environ Biol Fish 76:265–281Google Scholar
  54. Heg D, Bachar Z, Taborsky M (2005) Cooperative breeding and group structure in the Lake Tanganyika cichlid Neolamprologus savoryi. Ethology 111:1017–1043Google Scholar
  55. Hirschenhauser K, Taborsky M, Oliveira T, Canario AV, Oliveira RF (2004) A test of the ‘challenge hypothesis’ in cichlid fish: simulated partner and territory intruder experiments. Anim Behav 68:741–750Google Scholar
  56. Hochberg ME (1991) Viruses as costs to gregarious feeding in the Lepidoptera. Oikos 61:291–296Google Scholar
  57. Hoogland JL (1979) Aggression, ectoparasitism, and other possible costs of prairie dog (Sciuridae, Cynomys spp.) coloniality. Behaviour 69:1–35Google Scholar
  58. Janson CH, Goldsmith ML (1995) Predicting group size in primates: foraging costs and predation risks. Behav Ecol 6:326–336Google Scholar
  59. Jordan LA, Avolio C, Herbert-Read JE, Krause J, Rubenstein DI, Ward AJW (2010a) Group structure in a restricted entry system is mediated by both resident and joiner preferences. Behav Ecol Sociobiol 64:1099–1106Google Scholar
  60. Jordan LA, Wong MYL, Balshine S (2010b) The effects of familiarity and social hierarchy on group membership decisions in a social fish. Biol Lett 6:301–303Google Scholar
  61. Koenig WD, Dickinson JL (2004) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, CambridgeGoogle Scholar
  62. Konings A (1998) Cichlids in their natural habitat. Cichlid Press, El PasoGoogle Scholar
  63. Konings A (2005) Back to nature guide to Tanganyika cichlids. Cichlid Press, El PasoGoogle Scholar
  64. Kortet R, Hedrick AV, Vainikka A (2010) Parasitism, predation and the evolution of animal personalities. Ecol Lett 13:1449–1458PubMedGoogle Scholar
  65. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, New YorkGoogle Scholar
  66. Krause J, Ruxton GD (2010) Important topics in group living. In: Szekely T, Moore AJ, Komdeur J (eds) Social behaviour: genes, ecology and evolution. Cambridge University Press, Cambridge, pp 203–225Google Scholar
  67. Lindström Å (1989) Finch flock size and risk of hawk predation at a migratory stopover site. Auk 106:225–232Google Scholar
  68. Lipsitch M, Nowak MA, Ebert D, May RM (1995) The population dynamics of vertically and horizontally transmitted parasites. Proc R Soc Lond B 260:321–327Google Scholar
  69. Lipsitch M, Siller S, Nowak MA (1996) The evolution of virulence in pathogens with vertical and horizontal transmission. Int J Organ Evol 50:1729–1741Google Scholar
  70. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–88Google Scholar
  71. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org
  72. Maréchal C, Poll M (1991) Check-list of the freshwater fishes of Africa, Volume 4. NHBS, TotnesGoogle Scholar
  73. Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Funct Ecol 20:290–299Google Scholar
  74. Matsumoto K, Kohda M (1998) Inter-population variation in the mating system of a substrate-breeding cichlid in Lake Tanganyika. J Ethol 16:123–127Google Scholar
  75. Mboko SK, Kohda M (1995) Pale and dark dichromatism related to microhabitats in a herbivorous Tanganyikan cichlid fish, Telmatochromis temporalis. J Ethol 13:77–83Google Scholar
  76. McCallum H, Barlow N, Hone J (2001) How should pathogen transmission be modelled? Trends Ecol Evol 16:295–300PubMedGoogle Scholar
  77. Møller AP, Merino S, Brown CR, Roberson RJ (2001) Immune defense and host sociality: a comparative study of swallows and martins. Am Nat 158:136–145PubMedGoogle Scholar
  78. Montero D, Izquierdo MS, Tort L, Robaina L, Vergara JM (1999) High stocking density produces crowding stress altering some physiological and biochemical parameters in gilthead seabream, Sparus aurata, juveniles. Fish Physiol Biochem 20:53–60Google Scholar
  79. Norris K, Evans MR (2000) Ecological immunity: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26Google Scholar
  80. Nunn CL, Gittleman JL, Antonovics J (2000) Promiscuity and the primate immune system. Science 290:1168–1170PubMedGoogle Scholar
  81. Ortuno J, Esteban MA, Meseguer J (2001) Effects of short-term crowding stress on the gilthead seabream (Sparus aurata L.) innate immune response. Fish Shellfish Immunol 11:187–197PubMedGoogle Scholar
  82. Padgett DA, Glaser R (2003) How stress influences the immune response. Trends Immunol 24:444–448PubMedGoogle Scholar
  83. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290PubMedGoogle Scholar
  84. Poiani A (1992) Ectoparasitism as a possible cost of social life: a comparative analysis using Australian passerines (Passeriformes). Oecologia 92:429–441Google Scholar
  85. Poulin R (1991a) Group-living and infestation by ectoparasites in passerines. Condor 93:418–423Google Scholar
  86. Poulin R (1991b) Group-living and the richness of the parasite fauna in Canadian freshwater fishes. Oecologia 86:390–394Google Scholar
  87. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  88. Raeymaekers JAM, Hablützel PI, Grégoir AF, Bamps J, Roose AK, Vanhove MPM, Steenberge V, Pariselle A, Huyse T, Snoeks J, Volckaert FAM (2013) Contrasting parasite communities among allopatric colour morphs of the Lake Tanganyika cichlid Tropheus. BMC Biol 13:41Google Scholar
  89. Ranta E (1992) Gregariousness versus solitude—another look at parasite faunal richness in Canadian freshwater fishes. Oecologia 89:150–152Google Scholar
  90. Ridley M (1993) The red queen: sex and the evolution of human nature. Harper Perennial, New YorkGoogle Scholar
  91. Riehl C (2013) Evolutionary routes to non-kin cooperative breeding in birds. Proc R Soc Lond B 280:20132245Google Scholar
  92. Russell AF, Lummaa V (2009) Maternal effects in cooperative breeders: from hymenopterans to humans. Phil Trans R Soc Lond B 364:1143–1167Google Scholar
  93. Santangelo N, Bass AH (2006) New insights into neuropeptide modulation of aggression: field studies of arginine vasotocin in a territorial tropical damselfish. Proc R Soc Lond B 273:3085–3092Google Scholar
  94. Semple S, Cowlinshaw G, Bennett P (2002) Immune system evolution among anthropoid primates: parasites, injuries and predators. Proc R Soc Lond B 269:1031–1037Google Scholar
  95. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321PubMedGoogle Scholar
  96. Shibasaki T, Hotta M, Sugihara H, Wakabayashi I (1998) Brain vasopressin is involved in stress-induced suppression of immune function in the rat. Brain Res 808:84–92PubMedGoogle Scholar
  97. Smits JE, Williams TD (1999) Validation of immunotoxicology techniques in passerine chicks exposed to oil sands tailings water. Ecotoxicol Environ Saf 44:105–112PubMedGoogle Scholar
  98. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing techniques in studies of avian immunocompetence. Funct Ecol 13:567–572Google Scholar
  99. Spottiswoode CN (2008) Cooperative breeding and immunity: a comparative study of PHA response in African birds. Behav Ecol Sociobiol 62:963–974Google Scholar
  100. Stiver KA, Fitzpatrick JL, Desjardins JK, Balshine S (2004) Dispersal patterns and status change in a cooperatively breeding fish: evidence from microsatellite analyses and behavioural observations. J Fish Biol 65:91–105Google Scholar
  101. Stiver KA, Dierkes P, Taborksy M, Gibbs HL, Balshine S (2005) Relatedness and helping in fish: examining the theoretical predictions. Proc R Soc Lond B 272:1593–1599Google Scholar
  102. Stiver KA, Fitzpatrick J, Desjardins JK, Balshine S (2006) Sex differences in rates of territory joining and inheritance in a cooperatively breeding cichlid fish. Anim Behav 71:449–456Google Scholar
  103. Stiver KA, Desjardins JK, Fitzpatrick JL, Neff B, Quinn JS, Balshine S (2007) Evidence for size and sex-specific dispersal in a cooperatively breeding cichlid fish. Mol Ecol 16:2974–2984PubMedGoogle Scholar
  104. Sturmbauer C, Verheyen E, Meyer A (1994) Mitochondrial phylogeny of the Lamprologini, the major substrate spawning lineage of cichlid fishes from Lake Tanganyika in Eastern Africa. Mol Biol Evol 11:691–703PubMedGoogle Scholar
  105. Sturmbauer C, Salzburger W, Duftner N, Schelly R, Koblmüller S (2010) Evolutionary history of the Lake Tanganyika cichlid tribe Lamprologini (Teleostei: Perciformes) derived from mitochrondrial and nuclear DNA data. Mol Phylogenet Evol 57:266–284PubMedCentralPubMedGoogle Scholar
  106. Tort L (2011) Stress and immune modulation in fish. Dev Comp Immunol 35:1366–1375PubMedGoogle Scholar
  107. Uetz GW, Boyle J, Hieber CS, Wilcox RS (2002) Antipredator benefits of group living in colonial web-building spiders: the ‘early warning’ effect. Anim Behav 63:445–452Google Scholar
  108. Vanhove MPM, Snoeks J, Volckaert FAM, Huyse T (2010) First description of monogenean parasites in Lake Tananyika: the cichlid Simochromis diagramma (Teleostei, Cichlidae) harbours a high diversity of Gyrodactylus species (Platyhelminthes, Monogenea). Parasitology 138:364–380PubMedGoogle Scholar
  109. Vanhove MPM, Volckaert FAM, Pariselle A (2011) Ancryocephalidae (Monogenea) of Lake Tanganyika: I: four new species of Cichlidogyrus from Opthalmotilapia ventralis (Teleostei: cichlidae), the first record of this parasite family in the basin. Zoologia 23:253–263Google Scholar
  110. Watve MG, Jog MM (1997) Epidemic diseases and host clustering: an optimum cluster size ensures maximum survival. J Theor Biol 184:167–171Google Scholar
  111. Watve MG, Sukumar R (1995) Parasite abundance and diversity in mammals—correlates with host ecology. Proc Natl Acad Sci U S A 296:72–75Google Scholar
  112. Wilson K, Knell R, Boots M, Koch-Osborne J (2003) Group living and investment in immune defence: an interspecific analysis. J Anim Ecol 72:133–143Google Scholar
  113. Wingfield JC, Hegner RE, Dufty AM Jr, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846Google Scholar
  114. Wong MYL, Balshine S (2011) The evolution of cooperative breeding in the African cichlid fish, Neolamprologus pulcher. Biol Rev 86:511–530PubMedGoogle Scholar
  115. Wong MYL, Jordan LA, Marsh-Rollo S, St-Cyr S, Reynolds J, Stiver KA, Desjardins JK, Fitzpatrick JL, Balshine S (2012) Mating systems in cooperative breeders: the roles of resource limitation and conflict mitigation. Behav Ecol 23:521–530Google Scholar
  116. Wrona FJ, Dixon RWJ (1991) Group size and predation risk: a field analysis of encounter and dilution effects. Am Nat 137:186–201Google Scholar
  117. Yin Z, Lam TJ, Sin YM (1995) The effects of crowding stress on the non-specific immuneresponse in fancy carp (Cyprinus carpio L.). Fish Shellfish Immunol 5:519–529Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Constance M. O’Connor
    • 1
    Email author
  • Adam R. Reddon
    • 1
    • 4
  • Susan E. Marsh-Rollo
    • 1
  • Jennifer K. Hellmann
    • 2
  • Isaac Y. Ligocki
    • 2
  • Ian M. Hamilton
    • 2
    • 3
  • Sigal Balshine
    • 1
  1. 1.Aquatic Behavioural Ecology Laboratory, Department of Psychology, Neuroscience and BehaviourMcMaster UniversityHamiltonCanada
  2. 2.Department of Evolution, Ecology and Organismal BiologyThe Ohio State UniversityColumbusUSA
  3. 3.Department of MathematicsThe Ohio State UniversityColumbusUSA
  4. 4.Department of BiologyMcGill UniversityMontrealCanada

Personalised recommendations