Abstract
Life-history theory predicts that organisms optimize their resource allocation strategy to maximize lifetime reproductive success. Individuals can flexibly reallocate resources depending on their life-history stage, and environmental and physiological factors, which lead to variable life-history strategies even within species. Physiological trade-offs between immunity and reproduction are particularly relevant for long-lived species that need to balance current reproduction against future survival and reproduction, but their underlying mechanisms are poorly understood. A major unresolved issue is whether the first-line innate immune function is suppressed by reproductive investment. In this paper, we tested if reproductive investment is associated with the suppression of innate immunity, and how this potential trade-off is resolved depending on physiological state and residual reproductive value. We used long-lived capital-breeding female eiders (Somateria mollissima) as a model. We showed that the innate immune response, measured by plasma bacteria-killing capacity (BKC), was negatively associated with increasing reproductive investment, i.e., with increasing clutch size and advancing incubation stage. Females in a better physiological state, as indexed by low heterophil-to-lymphocyte (H/L) ratios, showed higher BKC during early incubation, but this capacity decreased as incubation progressed, whereas females in poorer state showed low BKC capacity throughout incubation. Although plasma BKC generally declined with increasing H/L ratios, this decrease was most pronounced in young females. Our results demonstrate that reproductive investment can suppress constitutive first-line immune defence in a long-lived bird, but the degree of immunosuppression depends on physiological state and age.
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Acknowledgments
We thank Heikki Eriksson, Ben Steele, Petteri Lehikoinen, Martin Seltmann, and James Montanari for their efforts in the field. We are also grateful to Tuomas Ojalehto for his valuable advice on performing BKC assays and two anonymous reviewers for constructive comments. Tvärminne Zoological Station provided excellent facilities. The study was funded by The Academy of Finland (Grant # 266208 to KJ and # 1265211 to Juha Merilä which supported the work of KN), The Finnish Cultural Foundation (KJ and KN), Walter and Andrée de Nottbeck foundation (SN), Societas pro Fauna et Flora Fennica (KN), Otto A. Malm foundation (KN), and the Swedish Cultural Foundation in Finland (MÖ).
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KN and KJ originally formulated the idea, SAN, MÖ, and KJ conducted fieldwork and the SAN performed laboratory analyses, KJ and KN analysed the data, all authors contributed to manuscript writing.
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Eider female handling procedures were approved by the Animal Experiment Board/State Provincial Office of Southern Finland (permit number ESAVI/1697/04.10.03/2012). Female trapping procedures also complied with the regulations of the Tvärminne Zoological Station. The ethics involved in female capture are explained in more detail by Kilpi et al. (2001).
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Communicated by Indrikis Krams.
S. A. Neggazi and K. Noreikiene contributed equally.
In this study we have investigated whether innate immune function is suppressed by the reproductive investment in a long-lived bird. We demonstrate for the first time that the innate immune response, measured as bacteria killing capacity of blood plasma, is negatively associated with increased reproductive investment in a wild bird. However, the degree of suppression of this first line of immune defence depends on both the health status and age of the bird.
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Neggazi, S.A., Noreikiene, K., Öst, M. et al. Reproductive investment is connected to innate immunity in a long-lived animal. Oecologia 182, 347–356 (2016). https://doi.org/10.1007/s00442-016-3657-7
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DOI: https://doi.org/10.1007/s00442-016-3657-7