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Heightened Exposure to Parasites Favors the Evolution of Immunity in Brood Parasitic Cowbirds

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Abstract

Immunologists and evolutionary biologists are interested in how the immune system evolves to fit an ecological niche. We studied the relationship between exposure to parasites and strength of immunity by investigating the response of two species of New World cowbirds (genus Molothrus, Icteridae), obligate brood parasites with contrasting life history strategies, to experimental arboviral infection. The South American shiny cowbird (M. bonariensis) is an extreme host-generalist that lays its eggs in the nests of >225 different avian species. The Central American bronzed cowbird (M. aeneus) is a relative host-specialist that lays its eggs preferentially in the nests of approximately 12 orioles in a single sister genus. West Nile virus provided a strong challenge and delineated immune differences between these species. The extreme host-generalist shiny cowbird, like the North American host-generalist, the brown-headed cowbird, showed significantly lower viremia to three arboviruses than related icterid species that were not brood parasites. The bronzed cowbird showed intermediate viremia. These findings support the interpretation that repeated exposure to a high diversity of parasites favors the evolution of enhanced immunity in brood parasitic cowbirds and makes them useful models for future studies of innate immunity.

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References

  • Adamo, S. A. (2004). How should behavioural ecologists interpret measurements of immunity? Animal Behaviour, 68, 1443–1449.

    Article  Google Scholar 

  • Apanius, V. (1998). Ontogeny of immune function. In J. M. Starck & R. E. Ricklefs (Eds.), Avian growth and development, evolution within the altricial-precocial spectrum (pp. 203–222). Oxford: Oxford University Press.

    Google Scholar 

  • Aspoeck, H. (2002). Ticks, insects, and other arthropods as pathogens and vectors. Parasiten und parasitäre Erkrankungen des Menschen im Mitteleuropa (pp. 397–445). Linz: Biologiezentrum des Oberösterreichischen Landesmuseums.

    Google Scholar 

  • Balakrishnan, C. N., & Sorenson, M. D. (2007). Dispersal ecology versus host specialization as determinants of ectoparasite distribution in brood parasitic indigobirds and their estrildid finch hosts. Molecular Ecology, 16(1), 217–229.

    Article  PubMed  CAS  Google Scholar 

  • Bartlett, C. M. (1993). Lice (Amblycera and Ischnocera) as vectors of Eulimdana Spp. (Nematoda, Filarioidea) in charadriiform birds and the necessity of short reproductive periods in adult worms. Journal of Parasitology, 79(1), 85–91.

    Article  Google Scholar 

  • Beletsky, L. (1996). The red-winged blackbird. The biology of a strongly polygynous songbird. San Diego: Academic Press.

  • Beletsky, L. D., & Orians, G. H. (1996). Red-winged blackbirds: Decision-making and reproductive success. Chicago: University of Chicago Press.

  • Bennett, G. F. (1995). International reference centre for avian hematozoa: A database available to the research community. Systematic Parasitology, 37, 237–238.

    Google Scholar 

  • Bize, P., Roulin, A., Tella, J. L., Bersier, L. F., & Richner, H. (2004). Additive effects of ectoparasites over reproductive attempts in the long-lived alpine swift. Journal of Animal Ecology, 73(6), 1080–1088.

    Article  Google Scholar 

  • Blount, J. D., Houston, D. C., Moller, A. P., & Wright, J. (2003). Do individual branches of immune defence correlate? A comparative case study of scavenging and non-scavenging birds. Oikos, 102(2), 340–350.

    Article  Google Scholar 

  • Brown, C. R., Brown, M. B., & Rannala, B. (1995). Ectoparasites reduce long-term survival of their avian host. Proceedings of the Royal Society of London Series B-Biological Sciences, 262(1365), 313–319.

    Article  Google Scholar 

  • Buehler, D. M. (2008). Bottlenecks, budgets and immunity: The costs and benefits of immune function over the annual cycle of red knots (Calidris canutus). Groningen: University of Groningen.

    Google Scholar 

  • Buehler, D. M., Piersma, T., & Tieleman, B. I. (2008). Captive and free-living red knots Calidris canutus exhibit differences in non-induced immunity that suggest different immune strategies in different environments. Journal of Avian Biology, 39(5), 560–566.

    Article  Google Scholar 

  • Chiles, R., & Reisen, W. (1998). A new enzyme immunoassay to detect antibodies to arboviruses in the blood of wild birds. Journal of Vector Ecology, 23, 123–135.

    PubMed  CAS  Google Scholar 

  • Clayton, D. H., & Tompkins, D. M. (1995). Comparative effects of mites and lice on the reproductive success of rock doves (Columba livia). Parasitology, 110, 195–206.

    Article  PubMed  Google Scholar 

  • Davies, N. B. (2000). Cuckoos, cowbirds, and other cheats. London: Poyser.

    Google Scholar 

  • Ehrlich, P. R., Dobkin, D. S., & Wheye, D. (1988). The birder’s handbook: A field guide to the natural history of North American birds. New York: Simon and Schuster.

    Google Scholar 

  • Ellison, K., & Lowther, P. E. (2009). Bronzed cowbird (Molothrus aeneus). In A. Poole (Ed.), The birds of North America online. Ithaca: Cornell Lab of Ornithology.

    Google Scholar 

  • Friedmann, H. (1929). The cowbirds: A study in the biology of social parasitism. Baltimore: Charles C. Thomas.

    Google Scholar 

  • Friedmann, H. (1963). Host relations of the parasitic cowbird. Washington, DC: Smithsonian Institution.

    Google Scholar 

  • Godoy-Vitorino, F., Ley, R. E., Gao, Z., Pei, Z. H., Ortiz-Zuazaga, H., Pericchi, L. R., et al. (2008). Bacterial community in the crop of the hoatzin, a Neotropical folivorous flying bird. Applied and Environmental Microbiology, 74(19), 5905–5912.

    Article  PubMed  CAS  Google Scholar 

  • Greiner, E. C., Bennett, G. F., White, E. M., & Combs, R. F. (1975). Distribution of the avian hematozoa of North America. Canadian Journal of Zoology, 53, 1762–1787.

    Article  PubMed  CAS  Google Scholar 

  • Hahn, D. C., Kogut, M. H., Genovese, K. J., He, H., & Summers, S. G. (2009). Ecological conditions favoring the evolution of stronger immune defenses. European Society of Evolutionary Biology. Turino, Italy: ESEB.

    Google Scholar 

  • Hahn, D. C., & O’Connor, R. J. (2002). Contrasting determinants of abundance in the ancestral and colonized ranges of an invasive species. In J. M. Scott, P. J. Heglund, & M. Raphael (Eds.), Predicting species occurrences: Issues of scale and accuracy (pp. 219–229). Covello, CA: Island Press.

    Google Scholar 

  • Hahn, D. C., & Price, R. D. (2001). Lice as probes. Trends in Ecology & Evolution, 16(8), 432–433.

    Article  Google Scholar 

  • Hahn, D. C., Price, R. D., & Osenton, P. C. (2000). Use of lice to identify cowbird hosts. Auk, 117(4), 943–951.

    Article  Google Scholar 

  • Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S., et al. (2002). Ecology—climate warming and disease risks for terrestrial and marine biota. Science, 296(5576), 2158–2162.

    Article  PubMed  CAS  Google Scholar 

  • Hintze, J. (1988). NCSS statistical software. Kaysville, UT.

  • Janeway, C. A., Travers, P., Walport, M., & Schlomchik, M. (2001). Immunobiology. New York: Garland Publishing.

    Google Scholar 

  • Jaramillo, A., & Burke, P. (1999). New world blackbirds: The icterids. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Johnsgard, P. A. (1997). The avian brood parasites. New York: Oxford University Press.

    Google Scholar 

  • Kilpatrick, A. M., LaDeau, S. L., & Marra, P. P. (2007). Ecology of west Nile virus transmission and its impact on birds in the western hemisphere. Auk, 124(4), 1121–1136.

    Article  Google Scholar 

  • Klasing, K. C., & Leshchinsky, T. V. (1998). Functions, costs, and benefits of the immune system during development and growth. In N. J. Adams & R. H. Slotow (Eds.), Proceedings of the 22nd international ornithological congress (pp. 2817–2835). Durban: BirdLife South Africa.

  • Komar, N., Langevin, S., Hinten, S., Nemeth, N., Edwards, E., Hettler, D., Davis, B., Bowen, R., & Bunning, M. (2003). Experimental infection of north American birds with the New York 1999 strain of West Nile virus. Emerging Infectious Diseases, 9, 311–322.

    PubMed  Google Scholar 

  • Kostecke, R. M., Ellison, K., & Summers, S. G. (2004). Continued range expansion by bronzed cowbirds in the southwestern United States. Southwestern Naturalist, 49(4), 487–492.

    Article  Google Scholar 

  • Kramer, L. D., Wolfe, T. M., Green, E. N., Chiles, R. E., Fallah, H., Fang, Y., et al. (2002). Detection of encephalitis viruses in mosquitoes (Diptera: Culicidae) and avian tissues. Journal of Medical Entomology, 39(2), 312–323.

    Article  PubMed  CAS  Google Scholar 

  • Kyle, P., & Kyle, G. (1990). An evaluation of the role of microbial flora in the salivary transfer technique for hand-rearing chimney swifts. In D. R. Ludwig (Ed.), Wildlife rehabilitation: Selected papers presented at the eighth symposium of the National Wildlife Rehabilitators Association, Ithaca, NY, March 21–25, 1990, pp. 65–72.

  • Lanyon, S. M. (1992). Interspecific brood parasitism in blackbirds (Icterinae)—a phylogenetic perspective. Science, 255(5040), 77–79.

    Article  PubMed  CAS  Google Scholar 

  • Lanyon, S. M., & Omland, K. E. (1999). A molecular phylogeny of the blackbirds (Icteridae): Five lineages revealed by cytochrome-b sequence data. Auk, 116(3), 629–639.

    Google Scholar 

  • Lehmann, T. (1993). Ectoparasites: Direct impact on host fitness. Parasitology Today, 9(1), 8–13.

    Article  PubMed  CAS  Google Scholar 

  • Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P. J., Ramey, R. R., Bircher, J. S., et al. (2008). Evolution of mammals and their gut microbes. Science, 320(5883), 1647–1651.

    Article  PubMed  CAS  Google Scholar 

  • Lindholm, A. K., Venter, G. J., & Euckermann, E. A. (1998). Persistence of passerine ectoparasites on the diederik cuckoo, Chrysococcyx caprius. Journal of Zoology London, 244, 145–153.

    Article  Google Scholar 

  • Lindstrom, K. M., Foufopoulos, J., Parn, H., & Wikelski, M. (2004). Immunological investments reflect parasite abundance in island populations of Darwin’s finches. Proceedings of the Royal Society of London Series B-Biological Sciences, 271(1547), 1513–1519.

    Article  Google Scholar 

  • Lowther, P. E. (1993). Brown-headed cowbird (Molothrus ater). In A. Poole (Ed.), The birds of North America online. http://bna.birds.cornell.edu/bna/species/047. Ithaca: Cornell Lab of Ornithology.

  • Lowther, P. E., & Post, W. (1999). Shiny Cowbird (Molothrus bonariensis). In A. Poole (Ed.), The birds of North America online. Ithaca: Cornell Lab of Ornithology.

    Google Scholar 

  • Ludwig, G. V., Calle, P. P., Mangiafico, J. A., Raphael, B. L., Danner, D. K., Hile, J. A., Clippinger, T. L., Smith, J. F., Cook, R. A., & McNamara, T. (2002). An outbreak of West Nile virus in a New York City captive wildlife population. American Journal of Tropical Medicine and Hygiene, 67, 67–75.

    PubMed  Google Scholar 

  • Martin, L. B., Weil, Z. M., & Nelson, R. J. (2007). Immune defense and reproductive pace of life in Peromyscus mice. Ecology, 88, 2516–2528.

    Article  PubMed  Google Scholar 

  • Mendes, L., Piersma, T., Hasselquist, D., Matson, K. D., & Ricklefs, R. E. (2006). Variation in the innate and acquired arms of the immune system among five shorebird species. Journal of Experimental Biology, 209(2), 284–291.

    Article  PubMed  Google Scholar 

  • Millet, S., Bennett, J., Lee, K. A., Hau, M., & Klasing, K. C. (2007). Quantifying and comparing constitutive immunity across avian species. Developmental and Comparative Immunology, 31, 188–201.

    Article  PubMed  CAS  Google Scholar 

  • Moller, A. P. (1997). Parasitism and the evolution of host life history. In D. H. Clayton & J. Moore (Eds.), Host-parasite evolution: General principles and avian models (pp. 105–127). Oxford: Oxford University Press.

    Google Scholar 

  • Norris, K., & Evans, M. R. (2000). Ecological immunology: Life history trade-offs and immune defense in birds. Behavioral Ecology, 11(1), 19–26.

    Article  Google Scholar 

  • Ortega, C. (1998). Cowbirds and other brood parasites. Tucson, AZ: University of Arizona Press.

    Google Scholar 

  • Payne, R. B. (1977). The ecology of brood parasitism in birds. Annual Review of Ecology and Systematics, 8, 1–28.

    Article  Google Scholar 

  • Price, R. D., Hellenthal, R. A., Palma, R. L., Johnson, K. P., & Clayton, D. H. (2003). The chewing lice: World checklist and biological overview (p. 501). Champagne, IL: Illinois Natural History Survey.

    Google Scholar 

  • Price, J. J., Lanyon, S. M., & Omland, K. E. (2009). Losses of female song with changes from tropical to temperate breeding in the New World blackbirds. Proceedings of the Royal Society B-Biological Sciences, 276(1664), 1971–1980.

    Article  Google Scholar 

  • Reisen, W. K., Chiles, R. E., Kramer, L. D., Martinez, V. M., & Eldridge, B. F. (2000). Method of infection does not alter the response of chicks and house finches to western equine encephalomyelitis and St. Louis encephalitis viruses. Journal of Medical Entomology, 37, 250–258.

    Article  PubMed  CAS  Google Scholar 

  • Reisen, W. K., Chiles, R. E., Martinez, V. M., Fang, Y., & Green, E. N. (2003). Experimental infection of California birds with western equine encephalomyelitis and St. Louis encephalitis viruses. Journal of Medical Entomology, 40(6), 968–982.

    Article  PubMed  CAS  Google Scholar 

  • Reisen, W. K., Fang, Y., & Martinez, V. M. (2005). Avian host and mosquito (Diptera: Culicidae) vector competence determine the efficiency of West Nile and St. Louis encephalitis virus transmission. Journal of Medical Entomology, 42, 367–375.

    Article  PubMed  CAS  Google Scholar 

  • Reisen, W. K., & Hahn, D. C. (2007). Comparison of immune responses of brown-headed cowbird and related blackbirds to West Nile and other mosquito-borne encephalitis viruses. Journal of Wildlife Diseases, 43(3), 439–449.

    PubMed  Google Scholar 

  • Reisen, W. K., Milby, M. M., Presser, S. B., & Hardy, J. L. (1992). Ecology of mosquitos and St. Louis encephalitis virus in the Los Angeles Basin of California, 1987–1990. Journal of Medical Entomology, 29(4), 582–598.

    PubMed  CAS  Google Scholar 

  • Rothstein, S. I., & Robinson, S. K. (Eds.). (1998). Parasitic birds and their hosts: Studies in coevolution. New York: Oxford University Press.

    Google Scholar 

  • SAS Institute. (1999). SAS/STAT user’s guide: Version 8. Cary, NC.

  • Schmid-Hempel, P. (2003). Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London Series B-Biological Sciences, 270(1513), 357–366.

    Article  Google Scholar 

  • Schmid-Hempel, P., & Ebert, D. (2003). On the evolutionary ecology of specific immune defence. Trends in Ecology & Evolution, 18, 27–32.

    Article  Google Scholar 

  • Schulenburg, H., Kurtz, J., Moret, Y., & Siva-Jothy, M. T. (2009). Introduction. Ecological immunology. Philosophical Transactions of the Royal Society B-Biological Sciences, 364(1513), 3–14.

    Article  Google Scholar 

  • Schwartz, M. W., Iverson, L. R., Prasad, A. M., Matthews, S. N., & O’Connor, R. J. (2006). Predicting extinctions as a result of climate change. Ecology, 87(7), 1611–1615.

    Article  PubMed  Google Scholar 

  • Searcy, W. A., & Yasukawa, K. (1995). Polygyny and sexual selection in red-winged blackbirds. Princeton: Princeton University Press.

    Google Scholar 

  • Searcy, W. A., Yasukawa, K., & Lanyon, S. (1999). Evolution of polygyny in the ancestors of red-winged blackbirds. Auk, 116(1), 5–19.

    Google Scholar 

  • Sheldon, B. C., & Verhulst, S. (1996). Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution, 11(8), 317–321.

    Article  CAS  Google Scholar 

  • Tieleman, B. I., Horrocks, N. P. D., Matson, K. D., Grizard, S., & Salles, J. F. (2011). How microbes shape birds and their eggs: Matching pathogen pressure and protection. Society for Integrative and Comparative Biology. Salt Lake City, UT.

  • Webster, M. S. (1992). Sexual dimorphism, mating system, and body size in New World blackbirds (Icterinae). Evolution, 46(6), 1621–1641.

    Article  Google Scholar 

  • Wheeler, S. S., Barker, C. M., Armijos, M. V., Carroll, B. D., Husted, S. R., & Reisen, W. K. (2009). Differential impact of West Nile virus on California birds. The Condor, 111, 1–20.

    Article  PubMed  Google Scholar 

  • Zuk, M., & Stoehr, A. M. (2002). Immune defense and host life history. American Naturalist, 160, S9–S22.

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Katsi Ramos Alvarez and Marilyn Colon, Division Recursos Terrestre, Puerto Rico for making shiny cowbirds available and arranging transport, and Scott Summers, The Nature Conservancy of Texas, for making bronzed cowbirds available and arranging transport. This research was funded, in part, by Research Grants RO1-39483, RO1-AI47855, and AI55607 from the National Institutes of Allergy and Infectious Diseases, NIH, the Coachella Valley and Kern Mosquito and Vector Control Districts, special funds for the Mosquito Research Program allocated annually through the Division of Agriculture and Natural Resources, University of California, and by base funds from USGS-Patuxent Wildlife Research Center. We thank staff of the Center for Vectorborne Diseases for excellent technical support: V.M. Martinez, H.D. Lothrop, S.S. Wheeler and B.D. Carroll assisted with bird collections; V.M. Martinez assisted with bird maintenance and bleeding; and Y. Fang, M. Shafii, S. Garcia, R.E. Chiles and S. Ashtari assisted with laboratory diagnostics. We thank R.B. Payne, S.M. Lanyon, D. Mock, and two anonymous reviewers for helpful comments on the manuscript. Use of trade, product, or firm names does not imply endorsement by the U.S. Government.

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  1. USGS-Patuxent Wildlife Research Center, Laurel, MD, 20708, USA

    D. Caldwell Hahn

  2. Center for Vectorborne Diseases and Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, CA, 95616, USA

    William K. Reisen

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Hahn, D.C., Reisen, W.K. Heightened Exposure to Parasites Favors the Evolution of Immunity in Brood Parasitic Cowbirds. Evol Biol 38, 214–224 (2011). https://doi.org/10.1007/s11692-011-9112-0

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