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Philos Trans R Soc Lond B Biol Sci
2023 Jul 31;3781882:20220127. doi: 10.1098/rstb.2022.0127.
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Ontogeny of immunity and potential implications for co-infection.
Ramsay C, Rohr JR.
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Immunity changes through ontogeny and can mediate facilitative and inhibitory interactions among co-infecting parasite species. In amphibians, most immune memory is not carried through metamorphosis, leading to variation in the complexity of immune responses across life stages. To test if the ontogeny of host immunity might drive interactions among co-infecting parasites, we simultaneously exposed Cuban treefrogs (Osteopilus septentrionalis) to a fungus (Batrachochytrium dendrobaditis, Bd) and a nematode (Aplectana hamatospicula) at tadpole, metamorphic and post-metamorphic life stages. We measured metrics of host immunity, host health and parasite abundance. We predicted facilitative interactions between co-infecting parasites as the different immune responses hosts mount to combat these infectious are energetically challenging to mount simultaneously. We found ontogenetic differences in IgY levels and cellular immunity but no evidence that metamorphic frogs were more immunosuppressed than tadpoles. There was also little evidence that these parasites facilitated one another and no evidence that A. hamatospicula infection altered host immunity or health. However, Bd, which is known to be immunosuppressive, decreased immunity in metamorphic frogs. This made metamorphic frogs both less resistant and less tolerant of Bd infection than the other life stages. These findings indicate that changes in immunity altered host responses to parasite exposures throughout ontogeny. This article is part of the theme issue 'Amphibian immunity: stress, disease and ecoimmunology'.
Abbas,
Functional diversity of helper T lymphocytes.
1996, Pubmed
Abbas,
Functional diversity of helper T lymphocytes.
1996,
Pubmed Abu Bakar,
Susceptibility to disease varies with ontogeny and immunocompetence in a threatened amphibian.
2016,
Pubmed Berger,
Th1 and Th2 responses: what are they?
2000,
Pubmed Berger,
Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.
1998,
Pubmed Blanco,
Immune response to fungal infections.
2008,
Pubmed Boucontet,
A Model of Superinfection of Virus-Infected Zebrafish Larvae: Increased Susceptibility to Bacteria Associated With Neutrophil Death.
2018,
Pubmed Boyle,
Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay.
2004,
Pubmed Budischak,
Resource limitation alters the consequences of co-infection for both hosts and parasites.
2015,
Pubmed Butcher,
Senescence in innate immune responses: reduced neutrophil phagocytic capacity and CD16 expression in elderly humans.
2001,
Pubmed Cattadori,
Peak shift and epidemiology in a seasonal host-nematode system.
2005,
Pubmed Cattadori,
Variation in host susceptibility and infectiousness generated by co-infection: the myxoma-Trichostrongylus retortaeformis case in wild rabbits.
2007,
Pubmed Clerc,
Age affects antibody levels and anthelmintic treatment efficacy in a wild rodent.
2019,
Pubmed Cramp,
First line of defence: the role of sloughing in the regulation of cutaneous microbes in frogs.
2014,
Pubmed Ezenwa,
Hidden consequences of living in a wormy world: nematode‐induced immune suppression facilitates tuberculosis invasion in African buffalo.
2010,
Pubmed Ezenwa,
Epidemiology. Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales.
2015,
Pubmed Fites,
The invasive chytrid fungus of amphibians paralyzes lymphocyte responses.
2013,
Pubmed
,
Xenbase Fites,
Inhibition of local immune responses by the frog-killing fungus Batrachochytrium dendrobatidis.
2014,
Pubmed
,
Xenbase Fülöp,
Signal transduction changes in granulocytes and lymphocytes with ageing.
1994,
Pubmed Gause,
The immune response to parasitic helminths: insights from murine models.
2003,
Pubmed Graham,
Ecological rules governing helminth-microparasite coinfection.
2008,
Pubmed Hornef,
Ontogeny of intestinal epithelial innate immune responses.
2014,
Pubmed Kilpatrick,
The ecology and impact of chytridiomycosis: an emerging disease of amphibians.
2010,
Pubmed Knutie,
Host resistance and tolerance of parasitic gut worms depend on resource availability.
2017,
Pubmed Knutie,
Early-Life Diet Affects Host Microbiota and Later-Life Defenses Against Parasites in Frogs.
2017,
Pubmed Langhammer,
Susceptibility to the amphibian chytrid fungus varies with ontogeny in the direct-developing frog, Eleutherodactylus coqui.
2014,
Pubmed Lello,
Competition and mutualism among the gut helminths of a mammalian host.
2004,
Pubmed McMahon,
Transition of chytrid fungus infection from mouthparts to hind limbs during amphibian metamorphosis.
2015,
Pubmed McMahon,
Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression.
2014,
Pubmed Miller,
The aging immune system: primer and prospectus.
1996,
Pubmed Paul,
How are T(H)2-type immune responses initiated and amplified?
2010,
Pubmed Pedersen,
Emphasizing the ecology in parasite community ecology.
2007,
Pubmed Robert,
Comparative and developmental study of the immune system in Xenopus.
2009,
Pubmed
,
Xenbase Rollins-Smith,
Antimicrobial peptide defenses against pathogens associated with global amphibian declines.
2002,
Pubmed Rollins-Smith,
Metamorphosis and the amphibian immune system.
1998,
Pubmed Romani,
Immunity to fungal infections.
2011,
Pubmed Rosenblum,
Genome-wide transcriptional response of Silurana (Xenopus) tropicalis to infection with the deadly chytrid fungus.
2009,
Pubmed
,
Xenbase Roznik,
Elucidating mechanisms of invasion success: effects of parasite removal on growth and survival rates of invasive and native frogs.
2020,
Pubmed Sears,
Host life history and host-parasite syntopy predict behavioural resistance and tolerance of parasites.
2015,
Pubmed Smith,
Type 2 innate immunity in helminth infection is induced redundantly and acts autonomously following CD11c(+) cell depletion.
2012,
Pubmed Sow,
Ontogeny of the immune response in the ovine lung.
2012,
Pubmed Stutz,
Using multi-response models to investigate pathogen coinfections across scales: insights from emerging diseases of amphibians.
2018,
Pubmed Swanson,
Coinfections acquired from ixodes ticks.
2006,
Pubmed Vhora,
New host and distribution records for Aplectana hamatospicula (Ascaridida: Cosmocercidae) in Gastrophryne olivacea (Anura: Microhylidae) from the Great Plains U.S.A.
2013,
Pubmed Wake,
Colloquium paper: are we in the midst of the sixth mass extinction? A view from the world of amphibians.
2008,
Pubmed Woolhouse,
A theoretical framework for the immunoepidemiology of helminth infection.
1992,
Pubmed Zelante,
IL-17/Th17 in anti-fungal immunity: what's new?
2009,
Pubmed