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Reduced immune function predicts disease susceptibility in frogs infected with a deadly fungal pathogen.

Savage AE, Terrell KA, Gratwicke B, Mattheus NM, Augustine L, Fleischer RC - Conserv Physiol (2016)

Bottom Line: However, neither group differed from Bd-negative control frogs.The low BKA values in dying frogs compared with infected individuals without disease signs suggests that complement activity might signify different immunogenetic backgrounds or gene-by-environment interactions between the host, Bd and abiotic factors.We conclude that protein complement activity might be a useful predictor of Bd susceptibility and might help to explain differential disease outcomes in natural amphibian populations.

View Article: PubMed Central - PubMed

Affiliation: Center for Conservation and Evolutionary Genetics.

ABSTRACT
The relationship between amphibian immune function and disease susceptibility is of primary concern given current worldwide declines linked to the pathogenic fungus Batrachochytrium dendrobatidis (Bd). We experimentally infected lowland leopard frogs (Lithobates yavapaiensis) with Bd to test the hypothesis that infection causes physiological stress and stimulates humoral and cell-mediated immune function in the blood. We measured body mass, the ratio of circulating neutrophils to lymphocytes (a known indicator of physiological stress) and plasma bacterial killing ability (BKA; a measure of innate immune function). In early exposure (1-15 days post-infection), stress was elevated in Bd-positive vs. Bd-negative frogs, whereas other metrics were similar between the groups. At later stages (29-55 days post-infection), stress was increased in Bd-positive frogs with signs of chytridiomycosis compared with both Bd-positive frogs without disease signs and uninfected control frogs, which were similar to each other. Infection decreased growth during the same period, demonstrating that sustained resistance to Bd is energetically costly. Importantly, BKA was lower in Bd-positive frogs with disease than in those without signs of chytridiomycosis. However, neither group differed from Bd-negative control frogs. The low BKA values in dying frogs compared with infected individuals without disease signs suggests that complement activity might signify different immunogenetic backgrounds or gene-by-environment interactions between the host, Bd and abiotic factors. We conclude that protein complement activity might be a useful predictor of Bd susceptibility and might help to explain differential disease outcomes in natural amphibian populations.

No MeSH data available.


Related in: MedlinePlus

(A) Mean Batrachochytrium dendrobatidis (Bd) infection intensity [measured as genome equivalents (GE)] in dying (filled circles, n = 12) and surviving frogs (open circles, n = 37) measured weekly from 7 to 55 days post-infection (DPI). (B) Change in Bd infection intensity (value at time of euthanasia minus value at the most recent weekly sampling) for Bd-exposed frogs euthanized 1–15 DPI (pink, n = 18) and Bd-infected frogs surviving 29–55 DPI with (blue, n = 12) or without (green, n = 19) signs of chytridiomycosis. All values are shown ±SEM.
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COW011F1: (A) Mean Batrachochytrium dendrobatidis (Bd) infection intensity [measured as genome equivalents (GE)] in dying (filled circles, n = 12) and surviving frogs (open circles, n = 37) measured weekly from 7 to 55 days post-infection (DPI). (B) Change in Bd infection intensity (value at time of euthanasia minus value at the most recent weekly sampling) for Bd-exposed frogs euthanized 1–15 DPI (pink, n = 18) and Bd-infected frogs surviving 29–55 DPI with (blue, n = 12) or without (green, n = 19) signs of chytridiomycosis. All values are shown ±SEM.

Mentions: Infection intensity rose steadily over time, remained elevated throughout the remainder of the experiment, and was not significantly different between surviving and dying frogs (Fig. 1A; Supplementary Appendix 1 and Supplementary Fig. 1), consistent with field studies of Bd in natural L. yavapaiensis populations (Savage et al., 2011, 2015). From day 29 until 55 DPI, dying frogs showed a non-significant trend towards higher infection loads compared with surviving frogs, with the exception of 42 DPI when all infected frogs had a significant reduction in infection intensity (q ≥ 5.20, P ≤ 0.02; Fig. 1A). Based on our qualitative observations that skin shedding was most severe in the week before 42 DPI, we hypothesize that this reduction in zoospore load resulted from a high turnover of epidermis. However, we did not collect quantifiable information on skin shedding. Infection intensity did not change significantly during the week before euthanasia for any infected group (Fig. 1B), consistent with previous observations that Bd zoospore load does not reliably predict host mortality in L. yavapaiensis (Savage et al., 2011, 2015).Figure 1:


Reduced immune function predicts disease susceptibility in frogs infected with a deadly fungal pathogen.

Savage AE, Terrell KA, Gratwicke B, Mattheus NM, Augustine L, Fleischer RC - Conserv Physiol (2016)

(A) Mean Batrachochytrium dendrobatidis (Bd) infection intensity [measured as genome equivalents (GE)] in dying (filled circles, n = 12) and surviving frogs (open circles, n = 37) measured weekly from 7 to 55 days post-infection (DPI). (B) Change in Bd infection intensity (value at time of euthanasia minus value at the most recent weekly sampling) for Bd-exposed frogs euthanized 1–15 DPI (pink, n = 18) and Bd-infected frogs surviving 29–55 DPI with (blue, n = 12) or without (green, n = 19) signs of chytridiomycosis. All values are shown ±SEM.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4834730&req=5

COW011F1: (A) Mean Batrachochytrium dendrobatidis (Bd) infection intensity [measured as genome equivalents (GE)] in dying (filled circles, n = 12) and surviving frogs (open circles, n = 37) measured weekly from 7 to 55 days post-infection (DPI). (B) Change in Bd infection intensity (value at time of euthanasia minus value at the most recent weekly sampling) for Bd-exposed frogs euthanized 1–15 DPI (pink, n = 18) and Bd-infected frogs surviving 29–55 DPI with (blue, n = 12) or without (green, n = 19) signs of chytridiomycosis. All values are shown ±SEM.
Mentions: Infection intensity rose steadily over time, remained elevated throughout the remainder of the experiment, and was not significantly different between surviving and dying frogs (Fig. 1A; Supplementary Appendix 1 and Supplementary Fig. 1), consistent with field studies of Bd in natural L. yavapaiensis populations (Savage et al., 2011, 2015). From day 29 until 55 DPI, dying frogs showed a non-significant trend towards higher infection loads compared with surviving frogs, with the exception of 42 DPI when all infected frogs had a significant reduction in infection intensity (q ≥ 5.20, P ≤ 0.02; Fig. 1A). Based on our qualitative observations that skin shedding was most severe in the week before 42 DPI, we hypothesize that this reduction in zoospore load resulted from a high turnover of epidermis. However, we did not collect quantifiable information on skin shedding. Infection intensity did not change significantly during the week before euthanasia for any infected group (Fig. 1B), consistent with previous observations that Bd zoospore load does not reliably predict host mortality in L. yavapaiensis (Savage et al., 2011, 2015).Figure 1:

Bottom Line: However, neither group differed from Bd-negative control frogs.The low BKA values in dying frogs compared with infected individuals without disease signs suggests that complement activity might signify different immunogenetic backgrounds or gene-by-environment interactions between the host, Bd and abiotic factors.We conclude that protein complement activity might be a useful predictor of Bd susceptibility and might help to explain differential disease outcomes in natural amphibian populations.

View Article: PubMed Central - PubMed

Affiliation: Center for Conservation and Evolutionary Genetics.

ABSTRACT
The relationship between amphibian immune function and disease susceptibility is of primary concern given current worldwide declines linked to the pathogenic fungus Batrachochytrium dendrobatidis (Bd). We experimentally infected lowland leopard frogs (Lithobates yavapaiensis) with Bd to test the hypothesis that infection causes physiological stress and stimulates humoral and cell-mediated immune function in the blood. We measured body mass, the ratio of circulating neutrophils to lymphocytes (a known indicator of physiological stress) and plasma bacterial killing ability (BKA; a measure of innate immune function). In early exposure (1-15 days post-infection), stress was elevated in Bd-positive vs. Bd-negative frogs, whereas other metrics were similar between the groups. At later stages (29-55 days post-infection), stress was increased in Bd-positive frogs with signs of chytridiomycosis compared with both Bd-positive frogs without disease signs and uninfected control frogs, which were similar to each other. Infection decreased growth during the same period, demonstrating that sustained resistance to Bd is energetically costly. Importantly, BKA was lower in Bd-positive frogs with disease than in those without signs of chytridiomycosis. However, neither group differed from Bd-negative control frogs. The low BKA values in dying frogs compared with infected individuals without disease signs suggests that complement activity might signify different immunogenetic backgrounds or gene-by-environment interactions between the host, Bd and abiotic factors. We conclude that protein complement activity might be a useful predictor of Bd susceptibility and might help to explain differential disease outcomes in natural amphibian populations.

No MeSH data available.


Related in: MedlinePlus