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Obligate Brood Parasites Show More Functionally Effective Innate Immune Responses: An Eco-immunological Hypothesis

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Abstract

Immune adaptations of obligate brood parasites attracted interest when three New World cowbird species (Passeriformes, Icteridae, genus Molothrus) proved unusually resistant to West Nile virus. We have used cowbirds as models to investigate the eco-immunological hypothesis that species in parasite-rich environments characteristically have enhanced immunity as a life history adaptation. As part of an ongoing program to understand the cowbird immune system, in this study we measured degranulation and oxidative burst, two fundamental responses of the innate immune system. Innate immunity provides non-specific, fast-acting defenses against a variety of invading pathogens, and we hypothesized that innate immunity experiences particularly strong selection in cowbirds, because their life history strategy exposes them to diverse novel and unpredictable parasites. We compared the relative effectiveness of degranulation and oxidative burst responses in two cowbird species and one related, non-parasitic species. Both innate immune defenses were significantly more functionally efficient in the two parasitic cowbird species than in the non-parasitic red-winged blackbird (Icteridae, Agelaius phoeniceus). Additionally, both immune defenses were more functionally efficient in the brown-headed cowbird (M. ater), an extreme host-generalist brood parasite, than in the bronzed cowbird (M. aeneus), a moderate host-specialist with lower exposure to other species and their parasites. Thus the relative effectiveness of these two innate immune responses corresponds to the diversity of parasites in the niche of each species and to their relative resistance to WNV. This study is the first use of these two specialized assays in a comparative immunology study of wild avian species.

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Notes

  1. Western equine encephalomyelitis virus (Togaviridae, Alphavirus, WEEV).

  2. St. Louis encephalitis virus (Flaviviridae, Flavivirus, SLEV).

  3. WNV and WEEV.

  4. “Parasite” is used here in its widest sense, including viruses, bacteria, protists, and eukaryotes (Schulenburg et al. 2009).

  5. NADPH = reduced NADP (Nicotinamide adenine dinucleotide phosphate).

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Acknowledgments

This work was supported in part by USGS—Patuxent Wildlife Research Center and by USDA—ARS-Southern Plains Agricultural Research Center. We thank The Nature Conservancy of Texas and Fort Hood for assistance. Use of trade, product, or firm names does not imply endorsement by the US Government. We appreciate helpful comments on the manuscript from E. Hofmeister and 2 anonymous reviewers.

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  1. USGS-Patuxent Wildlife Research Center, 12100 Beech Forest Road, Laurel, MD, 20708, USA

    D. Caldwell Hahn

  2. The Nature Conservancy, Fort Hood, Killeen, TX, 76544, USA

    Scott G. Summers

  3. Southern Plains Agricultural Research Center, USDA-ARS, College Station, TX, 77845, USA

    Kenneth J. Genovese, Haiqi He & Michael H. Kogut

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  1. D. Caldwell Hahn
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  2. Scott G. Summers
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  5. Michael H. Kogut
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Correspondence to D. Caldwell Hahn.

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Hahn, D.C., Summers, S.G., Genovese, K.J. et al. Obligate Brood Parasites Show More Functionally Effective Innate Immune Responses: An Eco-immunological Hypothesis. Evol Biol 40, 554–561 (2013). https://doi.org/10.1007/s11692-013-9231-x

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