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

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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.

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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.

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  1. Adam R. Reddon

    Present address: Department of Biology, McGill University, 845 Sherbrooke Street West, Montreal, Quebec, H3A 0G4, Canada

Authors and Affiliations

  1. Aquatic Behavioural Ecology Laboratory, Department of Psychology, Neuroscience and Behaviour, McMaster University, 1280 Main Street West, Hamilton, Ontario, L8S 4K1, Canada

    Constance M. O’Connor, Adam R. Reddon, Susan E. Marsh-Rollo & Sigal Balshine

  2. Department of Evolution, Ecology and Organismal Biology, The Ohio State University, 318 West 12th Avenue, Columbus, OH, 43210, USA

    Jennifer K. Hellmann, Isaac Y. Ligocki & Ian M. Hamilton

  3. Department of Mathematics, The Ohio State University, 318 West 12th Avenue, Columbus, OH, 43210, USA

    Ian M. Hamilton

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O’Connor, C.M., Reddon, A.R., Marsh-Rollo, S.E. et al. A comparative study of an innate immune response in Lamprologine cichlid fishes. Naturwissenschaften 101, 839–849 (2014). https://doi.org/10.1007/s00114-014-1225-8

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