The Enemy of my Enemy is my Friend: Immune-Mediated Facilitation Contributes to Fitness of Co-Infecting Helminths

Abstract Our conceptual understanding of immune-mediated interactions between parasites is rooted in the theory of community ecology. One of the limitations of this approach is that most of the theory and empirical evidence has focused on resource or immune-mediated parasite competition and yet, there is ample evidence of positive interactions between species that could be generated by immune-mediated facilitation. Here, we develop an immuno-epidemiological framework and apply it to longitudinal infection data of two gastrointestinal helminths that infect a population of free-living rabbits to investigate, through model testing, the mechanisms of immune-mediated facilitation in dual infections. Simulations show that weakened, species-specific IgA antibody responses and unequal, albeit low, IgA cross-reactions explain higher parasite intensities in dual compared to single infections, for both helminths. Simulations also show that rabbits with dual infections shed more free-living stages that survive fort longer in the environment, implying greater onward transmission than hosts with single infections. These findings support the hypothesis that the two helminths interact through immune-mediated facilitation which contributes to greater fitness and the long-term co-circulation of both species in the host population.

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Work Title The Enemy of my Enemy is my Friend: Immune-Mediated Facilitation Contributes to Fitness of Co-Infecting Helminths
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Open Access
Creators
  1. Isabella Cattadori
  2. Chiara Vanalli
Keyword
  1. Intensity of infection, shedding, antibodies, cross-reaction, climate
License CC BY-NC-ND 4.0 (Attribution-NonCommercial-NoDerivatives)
Work Type Other
Publication Date September 2, 2021
DOI doi:10.26207/8q59-6j48
Deposited August 31, 2021

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Version 1
published

  • Created
  • Added Creator Isabella Cattadori
  • Added Params_GS_SI.txt
  • Added Params_GS_DU.txt
  • Added Params_TR_DU.txt
  • Added Params_TR_SI.txt
  • Added Input_variables.xlsx
  • Added Model_dual_infection.txt
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  • Deleted Params_TR_SI.txt
  • Updated Keyword Show Changes
    Keyword
    • Intensity of infection, shedding, antibodies, cross-reaction, climate
  • Added Creator Chiara Vanalli
  • Added READ_ME.txt
  • Added Params_GS_SI.txt
  • Added Params_GS_DU.txt
  • Added Params_TR_DU.txt
  • Added Params_TR_SI.txt
  • Added Input_variables.xlsx
  • Added Model_dual_infection.txt
  • Added Model_single_infection.txt
  • Added SParams_TR_SI.txt
  • Added SPDF.txt
  • Added Smeteo.txt
  • Added SParams_GS_SI.txt
  • Added SIgA_data.txt
  • Added SSI_model.m
  • Added Seffectivedays.txt
  • Added Spredcfrdata.m
  • Added Srabbit_data.txt
  • Added SSCRIPT.m
  • Added Sfittingfun.m
  • Added Dfittingfun.m
  • Added DParams_GSCO.txt
  • Added DCO_model.m
  • Added DSCRIPT.m
  • Added Deffectivedays.txt
  • Added DPDF.txt
  • Added Dmeteo.txt
  • Added Drabbit_data.txt
  • Added DIgA_data.txt
  • Added DParams_TRCO.txt
  • Added Dpredcfrdata.m
  • Updated Publication Date, License Show Changes
    Publication Date
    • 2021-09-02
    License
    • https://rightsstatements.org/page/InC/1.0/
  • Published
  • Updated

Version 2
published

  • Created
  • Updated License Show Changes
    License
    • https://rightsstatements.org/page/InC/1.0/
    • https://creativecommons.org/licenses/by-nc-nd/4.0/
  • Published
  • Updated

Version 3
published

  • Created
  • Updated Keyword, Description, Publication Date Show Changes
    Keyword
    • Intensity of infection, shedding, antibodies, cross-reaction, climate
    • Intensity of infection, free-living stages, antibodies, cross-reaction, rabbit, climate
    Description
    • Abstract
    • Our conceptual understanding of immune-mediated interactions between parasites is rooted in the theory of community ecology. One of the limitations of this approach is that most of the theory and empirical evidence has focused on resource or immune-mediated parasite competition and yet, there is ample evidence of positive interactions between species that could be generated by immune-mediated facilitation. Here, we develop an immuno-epidemiological framework and apply it to longitudinal infection data of two gastrointestinal helminths that infect a population of free-living rabbits to investigate, through model testing, the mechanisms of immune-mediated facilitation in dual infections. Simulations show that weakened, species-specific IgA antibody responses and unequal, albeit low, IgA cross-reactions explain higher parasite intensities in dual compared to single infections, for both helminths. Simulations also show that rabbits with dual infections shed more free-living stages that survive fort longer in the environment, implying greater onward transmission than hosts with single infections. These findings support the hypothesis that the two helminths interact through immune-mediated facilitation which contributes to greater fitness and the long-term co-circulation of both species in the host population.
    • 1. The conceptual understanding of immune-mediated interactions between parasites is rooted in the theory of community ecology. One of the limitations of this approach is that most of the theory and empirical evidence has focused on resource or immune-mediated competition between parasites and yet there is ample evidence of positive interactions that could be generated by immune-mediated facilitation.
    • 2. We developed an immuno-epidemiological model and applied it to longitudinal data of two gastrointestinal helminths in two rabbit populations to investigate, through model testing, how immune-mediated mechanisms of parasite regulation could explain the higher intensities of both helminths in rabbits with dual than single infections.
    • 3. The model framework was selected and calibrated on rabbit population A and then validated on the nearby rabbit population B to confirm the consistency of the findings and the generality of the mechanisms. Simulations suggested that the higher intensities in rabbits with dual infections could be explained by a weakened or low species-specific IgA response and an asymmetrical IgA cross-reaction.
    • 4. Simulations also indicated that rabbits with dual infections shed more free-living stages that survived for longer in the environment, implying greater transmission than stages from hosts with single infections. Temperature and humidity selectively affected the free-living stages of the two helminths.
    • 5. These patterns were comparable in the two rabbit populations and support the hypothesis that immune-mediated facilitation can contribute to greater parasite fitness and local persistence.
    Publication Date
    • 2021-09-02
    • 2022
  • Deleted DCO_model.m
  • Deleted Deffectivedays.txt
  • Deleted Dfittingfun.m
  • Deleted Dpredcfrdata.m
  • Deleted DSCRIPT.m
  • Deleted Input_variables.xlsx
  • Deleted Sfittingfun.m
  • Deleted SSI_model.m
  • Deleted SSCRIPT.m
  • Deleted Spredcfrdata.m
  • Deleted Seffectivedays.txt
  • Deleted Model_dual_infection.txt
  • Deleted Model_single_infection.txt
  • Deleted Params_GS_SI.txt
  • Deleted Params_GS_DU.txt
  • Deleted Params_TR_DU.txt
  • Deleted Params_TR_SI.txt
  • Deleted SParams_TR_SI.txt
  • Deleted SParams_GS_SI.txt
  • Deleted DParams_GSCO.txt
  • Deleted DParams_TRCO.txt
  • Deleted SPDF.txt
  • Deleted DPDF.txt
  • Deleted READ_ME.txt
  • Deleted Srabbit_data.txt
  • Deleted DIgA_data.txt
  • Deleted Dmeteo.txt
  • Deleted SIgA_data.txt
  • Deleted Smeteo.txt
  • Added Rabbit_Parasite_Climate Data.xlsx
  • Deleted Drabbit_data.txt
  • Added README.txt
  • Updated Publisher Show Changes
    Publisher
    • Journal of Animal Ecology
  • Updated License Show Changes
    License
    • https://creativecommons.org/licenses/by-nc-nd/4.0/
    • http://creativecommons.org/publicdomain/zero/1.0/
  • Published

Version 4
published

  • Created
  • Updated License Show Changes
    License
    • http://creativecommons.org/publicdomain/zero/1.0/
    • https://creativecommons.org/licenses/by-nc-nd/4.0/
  • Published

Version 5
published

  • Created
  • Added Dagostin et al. SI ScholarSphere.pdf
  • Deleted Dagostin et al. SI ScholarSphere.pdf
  • Added Dagostin et al. SI ScholarSphere.pdf
  • Published
  • Updated Work Title, Keyword, Publisher, and 2 more Show Changes
    Work Title
    • The Enemy of my Enemy is my Friend: Immune-Mediated Facilitation Contributes to Fitness of Co-Infecting Helminths
    • Data from: "The Enemy of my Enemy is my Friend: Immune-Mediated Facilitation Contributes to Fitness of Co-Infecting Helminths"
    Keyword
    • Intensity of infection, free-living stages, antibodies, cross-reaction, rabbit, climate
    • Intensity of infection, Free-living stages, Antibodies, Cross-reaction, Rabbit, Climate
    Publisher
    • Journal of Animal Ecology
    Description
    • Abstract
    • 1. The conceptual understanding of immune-mediated interactions between parasites is rooted in the theory of community ecology. One of the limitations of this approach is that most of the theory and empirical evidence has focused on resource or immune-mediated competition between parasites and yet there is ample evidence of positive interactions that could be generated by immune-mediated facilitation.
    • 2. We developed an immuno-epidemiological model and applied it to longitudinal data of two gastrointestinal helminths in two rabbit populations to investigate, through model testing, how immune-mediated mechanisms of parasite regulation could explain the higher intensities of both helminths in rabbits with dual than single infections.
    • 3. The model framework was selected and calibrated on rabbit population A and then validated on the nearby rabbit population B to confirm the consistency of the findings and the generality of the mechanisms. Simulations suggested that the higher intensities in rabbits with dual infections could be explained by a weakened or low species-specific IgA response and an asymmetrical IgA cross-reaction.
    • 4. Simulations also indicated that rabbits with dual infections shed more free-living stages that survived for longer in the environment, implying greater transmission than stages from hosts with single infections. Temperature and humidity selectively affected the free-living stages of the two helminths.
    • 5. These patterns were comparable in the two rabbit populations and support the hypothesis that immune-mediated facilitation can contribute to greater parasite fitness and local persistence.
    • 1. The conceptual understanding of immune-mediated interactions between parasites is rooted in the theory of community ecology. One of the limitations of this approach is that most of the theory and empirical evidence has focused on resource or immune-mediated competition between parasites and yet there is ample evidence of positive interactions that could be generated by immune-mediated facilitation.
    • 2. We developed an immuno-epidemiological model and applied it to longitudinal data of two gastrointestinal helminths in two rabbit populations to investigate, through model testing, how immune-mediated mechanisms of parasite regulation could explain the higher intensities of both helminths in rabbits with dual than single infections.
    • 3. The model framework was selected and calibrated on rabbit population A and then validated on the nearby rabbit population B to confirm the consistency of the findings and the generality of the mechanisms. Simulations suggested that the higher intensities in rabbits with dual infections could be explained by a weakened or low species-specific IgA response and an asymmetrical IgA cross-reaction.
    • 4. Simulations also indicated that rabbits with dual infections shed more free-living stages that survived for longer in the environment, implying greater transmission than stages from hosts with single infections. Temperature and humidity selectively affected the free-living stages of the two helminths.
    • 5. These patterns were comparable in the two rabbit populations and support the hypothesis that immune-mediated facilitation can contribute to greater parasite fitness and local persistence.
    Related URLs
    • https://doi.org/10.1111/1365-2656.13863