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Erschienen in: EcoHealth 4/2017

01.08.2017 | Original Contribution

Host Responses to Pathogen Priming in a Natural Songbird Host

verfasst von: Ariel E. Leon, Dana M. Hawley

Erschienen in: EcoHealth | Ausgabe 4/2017

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Abstract

Hosts in free-living populations can experience substantial variation in the frequency and dose of pathogen exposure, which can alter disease progression and protection from future exposures. In the house finch–Mycoplasma gallisepticum (MG) system, the pathogen is primarily transmitted via bird feeders, and some birds may be exposed to frequent low doses of MG while foraging. Here we experimentally determined how low dose, repeated exposures of house finches to MG influence host responses and protection from secondary high-dose challenge. MG-naive house finches were given priming exposures that varied in dose and total number. After quantifying host responses to priming exposures, all birds were given a secondary high-dose challenge to assess immunological protection. Dose, but not the number of exposures, significantly predicted both infection and disease severity following priming exposure. Furthermore, individuals given higher priming doses showed stronger protection upon secondary, high-dose challenge. However, even single low-dose exposures to MG, a proxy for what some birds likely experience in the wild while feeding, provided significant protection against a high-dose challenge. Our results suggest that bird feeders, which serve as sources of infection in the wild, may in some cases act as “immunizers,” with important consequences for disease dynamics.
Literatur
Zurück zum Zitat Adelman JS, Carter AW, Hopkins WA, Hawley DM (2013a) Deposition of pathogenic Mycoplasma gallisepticum onto bird feeders: host pathology is more important than temperature-driven increases in food intake. Biology Letters 9:20130594. doi:10.1098/rsbl.2013.0594 Adelman JS, Carter AW, Hopkins WA, Hawley DM (2013a) Deposition of pathogenic Mycoplasma gallisepticum onto bird feeders: host pathology is more important than temperature-driven increases in food intake. Biology Letters 9:20130594. doi:10.​1098/​rsbl.​2013.​0594
Zurück zum Zitat Adelman JS, Kirkpatrick L, Grodio JL, Hawley DM (2013b) House finch populations differ in early inflammatory signaling and pathogen tolerance at the peak of mycoplasma gallisepticum infection. The American Naturalist 181:674–689. doi:10.1086/670024 Adelman JS, Kirkpatrick L, Grodio JL, Hawley DM (2013b) House finch populations differ in early inflammatory signaling and pathogen tolerance at the peak of mycoplasma gallisepticum infection. The American Naturalist 181:674–689. doi:10.​1086/​670024
Zurück zum Zitat Aiello CM, Nussear KE, Esque TC, Emblidge PG, Sah P, Bansal S, Hudson PJ (2016) Host contact and shedding patterns clarify variation in pathogen exposure and transmission in threatened tortoise Gopherus agassizii : implications for disease modelling and management. Journal of Animal Ecology 85:829–842. doi: 10.1111/1365-2656.12511 CrossRefPubMed Aiello CM, Nussear KE, Esque TC, Emblidge PG, Sah P, Bansal S, Hudson PJ (2016) Host contact and shedding patterns clarify variation in pathogen exposure and transmission in threatened tortoise Gopherus agassizii : implications for disease modelling and management. Journal of Animal Ecology 85:829–842. doi: 10.​1111/​1365-2656.​12511 CrossRefPubMed
Zurück zum Zitat Altizer S, Davis AK, Cook KC, Cherry JJ (2004a) Age, sex, and season affect the risk of mycoplasmal conjunctivitis in a southeastern house finch population. Canadian Journal of Zoology 82:755–763. doi: 10.1139/z04-050 CrossRef Altizer S, Davis AK, Cook KC, Cherry JJ (2004a) Age, sex, and season affect the risk of mycoplasmal conjunctivitis in a southeastern house finch population. Canadian Journal of Zoology 82:755–763. doi: 10.​1139/​z04-050 CrossRef
Zurück zum Zitat Ben‐Ami F, Ebert D, Regoes RR (2010) Pathogen Dose Infectivity Curves as a Method to Analyze the Distribution of Host Susceptibility: A Quantitative Assessment of Maternal Effects after Food Stress and Pathogen Exposure. The American Naturalist 175:106–115. doi: 10.1086/648672 CrossRefPubMed Ben‐Ami F, Ebert D, Regoes RR (2010) Pathogen Dose Infectivity Curves as a Method to Analyze the Distribution of Host Susceptibility: A Quantitative Assessment of Maternal Effects after Food Stress and Pathogen Exposure. The American Naturalist 175:106–115. doi: 10.​1086/​648672 CrossRefPubMed
Zurück zum Zitat Best A, Tidbury H, White A, Boots M (2012) The evolutionary dynamics of within-generation immune priming in invertebrate hosts. Journal of The Royal Society Interface 10:20120887–20120887. doi: 10.1098/rsif.2012.0887 CrossRef Best A, Tidbury H, White A, Boots M (2012) The evolutionary dynamics of within-generation immune priming in invertebrate hosts. Journal of The Royal Society Interface 10:20120887–20120887. doi: 10.​1098/​rsif.​2012.​0887 CrossRef
Zurück zum Zitat Bonneaud C, Balenger SL, Russell AF, Zhang J, Hill GE, Edwards S V (2011) Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird. Proceedings of the National Academy of Sciences 108:7866–7871. doi: 10.1073/pnas.1018580108 CrossRef Bonneaud C, Balenger SL, Russell AF, Zhang J, Hill GE, Edwards S V (2011) Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird. Proceedings of the National Academy of Sciences 108:7866–7871. doi: 10.​1073/​pnas.​1018580108 CrossRef
Zurück zum Zitat Burnham KKP, Anderson DRD (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd ed., New York: Springer Burnham KKP, Anderson DRD (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd ed., New York: Springer
Zurück zum Zitat Dhondt AA, Altizer S, Cooch EG, Davis AK, Dobson A, Driscoll MJL, Hartup BK, Hawley DM, Hochachka WM, Hosseini PR, Jennelle CS, Kollias G V, Ley DH, Swarthout ECH, Sydenstricker K V (2005) Dynamics of a novel pathogen in an avian host: Mycoplasmal conjunctivitis in house finches. Acta Tropica 94:77–93. doi: 10.1016/j.actatropica.2005.01.009 CrossRefPubMed Dhondt AA, Altizer S, Cooch EG, Davis AK, Dobson A, Driscoll MJL, Hartup BK, Hawley DM, Hochachka WM, Hosseini PR, Jennelle CS, Kollias G V, Ley DH, Swarthout ECH, Sydenstricker K V (2005) Dynamics of a novel pathogen in an avian host: Mycoplasmal conjunctivitis in house finches. Acta Tropica 94:77–93. doi: 10.​1016/​j.​actatropica.​2005.​01.​009 CrossRefPubMed
Zurück zum Zitat Dhondt AA, Dhondt KV, Hawley DM, Jennelle CS (2007a) Experimental evidence for transmission of Mycoplasma gallisepticum in house finches by fomites. Avian Pathology 36:205–208. doi:10.1080/03079450701286277 Dhondt AA, Dhondt KV, Hawley DM, Jennelle CS (2007a) Experimental evidence for transmission of Mycoplasma gallisepticum in house finches by fomites. Avian Pathology 36:205–208. doi:10.​1080/​0307945070128627​7
Zurück zum Zitat Dhondt KV, Dhondt AA, Ley DH (2007b) Effects of route of inoculation on Mycoplasma gallisepticum infection in captive house finches. Avian Pathology 36:475–479. doi:10.1080/03079450701642016 Dhondt KV, Dhondt AA, Ley DH (2007b) Effects of route of inoculation on Mycoplasma gallisepticum infection in captive house finches. Avian Pathology 36:475–479. doi:10.​1080/​0307945070164201​6
Zurück zum Zitat Grenfell BT, Wilson K, Isham VS, Boyd HEG, Dietz K (1995) Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode–ruminant interactions as a case study. Parasitology 111:S135. doi: 10.1017/S0031182000075867 CrossRefPubMed Grenfell BT, Wilson K, Isham VS, Boyd HEG, Dietz K (1995) Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode–ruminant interactions as a case study. Parasitology 111:S135. doi: 10.​1017/​S003118200007586​7 CrossRefPubMed
Zurück zum Zitat Grodio JL, Dhondt K V, O’Connell PH, Schat KA (2008) Detection and quantification of Mycoplasma gallisepticum genome load in conjunctival samples of experimentally infected house finches (Carpodacus mexicanus) using real-time polymerase chain reaction. Avian Pathology 37:385–391. doi: 10.1080/03079450802216629 CrossRefPubMed Grodio JL, Dhondt K V, O’Connell PH, Schat KA (2008) Detection and quantification of Mycoplasma gallisepticum genome load in conjunctival samples of experimentally infected house finches (Carpodacus mexicanus) using real-time polymerase chain reaction. Avian Pathology 37:385–391. doi: 10.​1080/​0307945080221662​9 CrossRefPubMed
Zurück zum Zitat Grodio JL, Hawley DM, Osnas EE, Ley DH, Dhondt K V, Dhondt AA, Schat KA (2012) Pathogenicity and immunogenicity of three Mycoplasma gallisepticum isolates in house finches (Carpodacus mexicanus). Veterinary Microbiology 155:53–61. doi: 10.1016/j.vetmic.2011.08.003 CrossRefPubMed Grodio JL, Hawley DM, Osnas EE, Ley DH, Dhondt K V, Dhondt AA, Schat KA (2012) Pathogenicity and immunogenicity of three Mycoplasma gallisepticum isolates in house finches (Carpodacus mexicanus). Veterinary Microbiology 155:53–61. doi: 10.​1016/​j.​vetmic.​2011.​08.​003 CrossRefPubMed
Zurück zum Zitat Hawley DM, Grodio J, Frasca S, Kirkpatrick L, Ley DH (2011) Experimental infection of domestic canaries (Serinus canaria domestica) with Mycoplasma gallisepticum : a new model system for a wildlife disease. Avian Pathology 40:321–327. doi: 10.1080/03079457.2011.571660 CrossRefPubMed Hawley DM, Grodio J, Frasca S, Kirkpatrick L, Ley DH (2011) Experimental infection of domestic canaries (Serinus canaria domestica) with Mycoplasma gallisepticum : a new model system for a wildlife disease. Avian Pathology 40:321–327. doi: 10.​1080/​03079457.​2011.​571660 CrossRefPubMed
Zurück zum Zitat Johnson PTJ, Hoverman JT (2014) Heterogeneous hosts: how variation in host size, behaviour and immunity affects parasite aggregation. The Journal of animal ecology 1–10 (DOI: 10.1111/1365-2656.12215) Johnson PTJ, Hoverman JT (2014) Heterogeneous hosts: how variation in host size, behaviour and immunity affects parasite aggregation. The Journal of animal ecology 1–10 (DOI: 10.​1111/​1365-2656.​12215)
Zurück zum Zitat Ley DH, Berkhoff JE, McLaren JM (1996) Mycoplasma gallisepticum Isolated from House Finches (Carpodacus mexicanus) with Conjunctivitis. Avian Diseases 40:480. doi: 10.2307/1592250 CrossRefPubMed Ley DH, Berkhoff JE, McLaren JM (1996) Mycoplasma gallisepticum Isolated from House Finches (Carpodacus mexicanus) with Conjunctivitis. Avian Diseases 40:480. doi: 10.​2307/​1592250 CrossRefPubMed
Zurück zum Zitat Lillehoj HS (1988) Influence of inoculation dose, inoculation schedule, chicken age, and host genetics on disease susceptibility and development of resistance to Eimeria tenella infection. Avian diseases 32:437–44.CrossRefPubMed Lillehoj HS (1988) Influence of inoculation dose, inoculation schedule, chicken age, and host genetics on disease susceptibility and development of resistance to Eimeria tenella infection. Avian diseases 32:437–44.CrossRefPubMed
Zurück zum Zitat McElroy PD, Beier JC, Oster CN, Onyango FK, Oloo AJ, Lin X, Beadle C, Hoffman SL (1997) Dose- and time-dependent relations between infective Anopheles inoculation and outcomes of Plasmodium falciparum parasitemia among children in western Kenya. American journal of epidemiology 145:945–56.CrossRefPubMed McElroy PD, Beier JC, Oster CN, Onyango FK, Oloo AJ, Lin X, Beadle C, Hoffman SL (1997) Dose- and time-dependent relations between infective Anopheles inoculation and outcomes of Plasmodium falciparum parasitemia among children in western Kenya. American journal of epidemiology 145:945–56.CrossRefPubMed
Zurück zum Zitat McKinstry KK, Strutt TM, Buck A, Curtis JD, Dibble JP, Huston G, Tighe M, Hamada H, Sell S, Dutton RW, Swain SL (2009) IL-10 Deficiency Unleashes an Influenza-Specific Th17 Response and Enhances Survival against High-Dose Challenge. The Journal of Immunology 182:7353–7363. doi: 10.4049/jimmunol.0900657 CrossRefPubMedPubMedCentral McKinstry KK, Strutt TM, Buck A, Curtis JD, Dibble JP, Huston G, Tighe M, Hamada H, Sell S, Dutton RW, Swain SL (2009) IL-10 Deficiency Unleashes an Influenza-Specific Th17 Response and Enhances Survival against High-Dose Challenge. The Journal of Immunology 182:7353–7363. doi: 10.​4049/​jimmunol.​0900657 CrossRefPubMedPubMedCentral
Zurück zum Zitat Murphy K, Weaver C (2017) Janeway’s Immunobiology, 9th ed., Garland Science/Taylor & Francis Group, LLC Murphy K, Weaver C (2017) Janeway’s Immunobiology, 9th ed., Garland Science/Taylor & Francis Group, LLC
Zurück zum Zitat R Core team (2015) R Core Team. A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/. 55:275–286. R Core team (2015) R Core Team. A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://​www.​R-project.​org/​. 55:275–286.
Zurück zum Zitat Stranford SA, Skurnick J, Louria D, Osmond D, Chang S-Y, Sninsky J, Ferrari G, Weinhold K, Lindquist C, Levy JA (1999) Lack of infection in HIV-exposed individuals is associated with a strong CD8 + cell noncytotoxic anti-HIV response. Proceedings of the National Academy of Sciences 96:1030–1035. doi: 10.1073/pnas.96.3.1030 CrossRef Stranford SA, Skurnick J, Louria D, Osmond D, Chang S-Y, Sninsky J, Ferrari G, Weinhold K, Lindquist C, Levy JA (1999) Lack of infection in HIV-exposed individuals is associated with a strong CD8 + cell noncytotoxic anti-HIV response. Proceedings of the National Academy of Sciences 96:1030–1035. doi: 10.​1073/​pnas.​96.​3.​1030 CrossRef
Zurück zum Zitat Sydenstricker K V, Dhondt AA, Hawley DM, Jennelle CS, Kollias HW, Kollias G V (2006) Characterization of Experimental Mycoplasma gallisepticum Infection in Captive House Finch Flocks. Avian Diseases 50:39–44. doi: 10.1637/7403-062805R.1 CrossRefPubMed Sydenstricker K V, Dhondt AA, Hawley DM, Jennelle CS, Kollias HW, Kollias G V (2006) Characterization of Experimental Mycoplasma gallisepticum Infection in Captive House Finch Flocks. Avian Diseases 50:39–44. doi: 10.​1637/​7403-062805R.​1 CrossRefPubMed
Zurück zum Zitat Thomason CA, Leon A, Kirkpatrick LT, Belden LK, Hawley DM (2017) Eye of the Finch: characterization of the ocular microbiome of house finches in relation to mycoplasmal conjunctivitis. Environmental Microbiology. doi: 10.1111/1462-2920.13625 PubMed Thomason CA, Leon A, Kirkpatrick LT, Belden LK, Hawley DM (2017) Eye of the Finch: characterization of the ocular microbiome of house finches in relation to mycoplasmal conjunctivitis. Environmental Microbiology. doi: 10.​1111/​1462-2920.​13625 PubMed
Zurück zum Zitat Tidbury HJ, Pedersen AB, Boots M (2011) Within and transgenerational immune priming in an insect to a DNA virus. Proceedings Biological sciences/The Royal Society 278:871–6. doi: 10.1098/rspb.2010.1517 CrossRef Tidbury HJ, Pedersen AB, Boots M (2011) Within and transgenerational immune priming in an insect to a DNA virus. Proceedings Biological sciences/The Royal Society 278:871–6. doi: 10.​1098/​rspb.​2010.​1517 CrossRef
Zurück zum Zitat Vandenberg JD, Ramos M, Altre JA (1998) Dose-Response and Age- and Temperature-Related Susceptibility of the Diamondback Moth (Lepidoptera: Plutellidae) to Two Isolates of Beauveria bassiana (Hyphomycetes: Moniliaceae). Environmental Entomology 27:1017–1021. doi: 10.1093/ee/27.4.1017 CrossRef Vandenberg JD, Ramos M, Altre JA (1998) Dose-Response and Age- and Temperature-Related Susceptibility of the Diamondback Moth (Lepidoptera: Plutellidae) to Two Isolates of Beauveria bassiana (Hyphomycetes: Moniliaceae). Environmental Entomology 27:1017–1021. doi: 10.​1093/​ee/​27.​4.​1017 CrossRef
Zurück zum Zitat Woolhouse ME, Dye C, Etard JF, Smith T, Charlwood JD, Garnett GP, Hagan P, Hii JL, Ndhlovu PD, Quinnell RJ, Watts CH, Chandiwana SK, Anderson RM (1997) Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences of the United States of America 94:338–42.CrossRefPubMedPubMedCentral Woolhouse ME, Dye C, Etard JF, Smith T, Charlwood JD, Garnett GP, Hagan P, Hii JL, Ndhlovu PD, Quinnell RJ, Watts CH, Chandiwana SK, Anderson RM (1997) Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences of the United States of America 94:338–42.CrossRefPubMedPubMedCentral
Metadaten
Titel
Host Responses to Pathogen Priming in a Natural Songbird Host
verfasst von
Ariel E. Leon
Dana M. Hawley
Publikationsdatum
01.08.2017
Verlag
Springer US
Erschienen in
EcoHealth / Ausgabe 4/2017
Print ISSN: 1612-9202
Elektronische ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-017-1261-x

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