Ecological Factors Mediate Immunity and Parasitic Co-Infection in Sea Fan Octocorals

The interplay among environment, demography, and host-parasite interactions is a challenging frontier. In the ocean, fundamental changes are occurring due to anthropogenic pressures, including increased disease outbreaks on coral reefs. These outbreaks include multiple parasites, calling into questi...

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Main Authors: Allison M. Tracy, Ernesto Weil, Colleen A. Burge
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-01-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2020.608066/full
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spelling doaj-8c8622e2576640f58adcc372aae5aec92021-01-11T04:21:17ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-01-011110.3389/fimmu.2020.608066608066Ecological Factors Mediate Immunity and Parasitic Co-Infection in Sea Fan OctocoralsAllison M. Tracy0Ernesto Weil1Colleen A. Burge2Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, United StatesDepartment of Marine Sciences, University of Puerto Rico, Mayagüez, PR, United StatesInstitute of Marine and Environmental Technology, University of Maryland Baltimore County, Baltimore, MD, United StatesThe interplay among environment, demography, and host-parasite interactions is a challenging frontier. In the ocean, fundamental changes are occurring due to anthropogenic pressures, including increased disease outbreaks on coral reefs. These outbreaks include multiple parasites, calling into question how host immunity functions in this complex milieu. Our work investigates the interplay of factors influencing co-infection in the Caribbean sea fan octocoral, Gorgonia ventalina, using metrics of the innate immune response: cellular immunity and expression of candidate immune genes. We used existing copepod infections and live pathogen inoculation with the Aspergillus sydowii fungus, detecting increased expression of the immune recognition gene Tachylectin 5A (T5A) in response to both parasites. Cellular immunity increased by 8.16% in copepod infections compared to controls and single Aspergillus infections. We also detected activation of cellular immunity in reef populations, with a 13.6% increase during copepod infections. Cellular immunity was similar in the field and in the lab, increasing with copepod infections and not the fungus. Amoebocyte density and the expression of T5A and a matrix metalloproteinase (MMP) gene were also positively correlated across all treatments and colonies, irrespective of parasitic infection. We then assessed the scaling of immune metrics to population-level disease patterns and found random co-occurrence of copepods and fungus across 15 reefs in Puerto Rico. The results suggest immune activation by parasites may not alter parasite co-occurrence if factors other than immunity prevail in structuring parasite infection. We assessed non-immune factors in the field and found that sea fan colony size predicted infection by the copepod parasite. Moreover, the effect of infection on immunity was small relative to that of site differences and live coral cover, and similar to the effect of reproductive status. While additional immune data would shed light on the extent of this pattern, ecological factors may play a larger role than immunity in controlling parasite patterns in the wild. Parsing the effects of immunity and ecological factors in octocoral co-infection shows how disease depends on more than one host and one parasite and explores the application of co-infection research to a colonial marine organism.https://www.frontiersin.org/articles/10.3389/fimmu.2020.608066/fullecological immunityGorgonia ventalinaco-infectionhost demographyoctocoral
collection DOAJ
language English
format Article
sources DOAJ
author Allison M. Tracy
Ernesto Weil
Colleen A. Burge
spellingShingle Allison M. Tracy
Ernesto Weil
Colleen A. Burge
Ecological Factors Mediate Immunity and Parasitic Co-Infection in Sea Fan Octocorals
Frontiers in Immunology
ecological immunity
Gorgonia ventalina
co-infection
host demography
octocoral
author_facet Allison M. Tracy
Ernesto Weil
Colleen A. Burge
author_sort Allison M. Tracy
title Ecological Factors Mediate Immunity and Parasitic Co-Infection in Sea Fan Octocorals
title_short Ecological Factors Mediate Immunity and Parasitic Co-Infection in Sea Fan Octocorals
title_full Ecological Factors Mediate Immunity and Parasitic Co-Infection in Sea Fan Octocorals
title_fullStr Ecological Factors Mediate Immunity and Parasitic Co-Infection in Sea Fan Octocorals
title_full_unstemmed Ecological Factors Mediate Immunity and Parasitic Co-Infection in Sea Fan Octocorals
title_sort ecological factors mediate immunity and parasitic co-infection in sea fan octocorals
publisher Frontiers Media S.A.
series Frontiers in Immunology
issn 1664-3224
publishDate 2021-01-01
description The interplay among environment, demography, and host-parasite interactions is a challenging frontier. In the ocean, fundamental changes are occurring due to anthropogenic pressures, including increased disease outbreaks on coral reefs. These outbreaks include multiple parasites, calling into question how host immunity functions in this complex milieu. Our work investigates the interplay of factors influencing co-infection in the Caribbean sea fan octocoral, Gorgonia ventalina, using metrics of the innate immune response: cellular immunity and expression of candidate immune genes. We used existing copepod infections and live pathogen inoculation with the Aspergillus sydowii fungus, detecting increased expression of the immune recognition gene Tachylectin 5A (T5A) in response to both parasites. Cellular immunity increased by 8.16% in copepod infections compared to controls and single Aspergillus infections. We also detected activation of cellular immunity in reef populations, with a 13.6% increase during copepod infections. Cellular immunity was similar in the field and in the lab, increasing with copepod infections and not the fungus. Amoebocyte density and the expression of T5A and a matrix metalloproteinase (MMP) gene were also positively correlated across all treatments and colonies, irrespective of parasitic infection. We then assessed the scaling of immune metrics to population-level disease patterns and found random co-occurrence of copepods and fungus across 15 reefs in Puerto Rico. The results suggest immune activation by parasites may not alter parasite co-occurrence if factors other than immunity prevail in structuring parasite infection. We assessed non-immune factors in the field and found that sea fan colony size predicted infection by the copepod parasite. Moreover, the effect of infection on immunity was small relative to that of site differences and live coral cover, and similar to the effect of reproductive status. While additional immune data would shed light on the extent of this pattern, ecological factors may play a larger role than immunity in controlling parasite patterns in the wild. Parsing the effects of immunity and ecological factors in octocoral co-infection shows how disease depends on more than one host and one parasite and explores the application of co-infection research to a colonial marine organism.
topic ecological immunity
Gorgonia ventalina
co-infection
host demography
octocoral
url https://www.frontiersin.org/articles/10.3389/fimmu.2020.608066/full
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