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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

Principal components analysis (PCA) illustrating relationships among Batrachochytrium dendrobatidis (Bd) load, bacterial killing ability (BKA), growth rates and neutrophil/lymphocyte (N/L) ratios in uninfected frogs (n = 11, purple), Bd-infected individuals that did not develop chytridiomycosis (n = 10, green), Bd-infected individuals with chytridiomycosis (n = 6, blue) or Bd-exposed individuals euthanized during early infection, before disease signs occurred (n = 5, pink). Corresponding ellipses represent 68% confidence intervals for each group. Individuals with missing data for any of the above parameters were excluded from the PCA by necessity, resulting in smaller sample sizes.
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COW011F4: Principal components analysis (PCA) illustrating relationships among Batrachochytrium dendrobatidis (Bd) load, bacterial killing ability (BKA), growth rates and neutrophil/lymphocyte (N/L) ratios in uninfected frogs (n = 11, purple), Bd-infected individuals that did not develop chytridiomycosis (n = 10, green), Bd-infected individuals with chytridiomycosis (n = 6, blue) or Bd-exposed individuals euthanized during early infection, before disease signs occurred (n = 5, pink). Corresponding ellipses represent 68% confidence intervals for each group. Individuals with missing data for any of the above parameters were excluded from the PCA by necessity, resulting in smaller sample sizes.

Mentions: Frogs with missing data were excluded from PCA, resulting in smaller sample sizes for uninfected (n= 11), early infection (n = 5), surviving (n = 10) and dying (n = 6) frogs. Missing data were the result of limited blood volumes, which precluded N/L or BKA analysis for some frogs. Principal components 1 and 2 collectively accounted for 77% of the observed variation in the data set (Fig. 4). Visualization of these components revealed that dying frogs, survivors and control animals represented three distinct physiological groups. Frogs surviving infection were associated with high BKA, low N/L ratios, intermediate body mass gain and high zoospore loads. In contrast, frogs dying of chytridiomycosis exhibited low BKA, high N/L ratios, low body mass gain and high zoospore loads. Control frogs were associated with high body mass gain, but substantial variation in immune function.Figure 4:


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)

Principal components analysis (PCA) illustrating relationships among Batrachochytrium dendrobatidis (Bd) load, bacterial killing ability (BKA), growth rates and neutrophil/lymphocyte (N/L) ratios in uninfected frogs (n = 11, purple), Bd-infected individuals that did not develop chytridiomycosis (n = 10, green), Bd-infected individuals with chytridiomycosis (n = 6, blue) or Bd-exposed individuals euthanized during early infection, before disease signs occurred (n = 5, pink). Corresponding ellipses represent 68% confidence intervals for each group. Individuals with missing data for any of the above parameters were excluded from the PCA by necessity, resulting in smaller sample sizes.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

COW011F4: Principal components analysis (PCA) illustrating relationships among Batrachochytrium dendrobatidis (Bd) load, bacterial killing ability (BKA), growth rates and neutrophil/lymphocyte (N/L) ratios in uninfected frogs (n = 11, purple), Bd-infected individuals that did not develop chytridiomycosis (n = 10, green), Bd-infected individuals with chytridiomycosis (n = 6, blue) or Bd-exposed individuals euthanized during early infection, before disease signs occurred (n = 5, pink). Corresponding ellipses represent 68% confidence intervals for each group. Individuals with missing data for any of the above parameters were excluded from the PCA by necessity, resulting in smaller sample sizes.
Mentions: Frogs with missing data were excluded from PCA, resulting in smaller sample sizes for uninfected (n= 11), early infection (n = 5), surviving (n = 10) and dying (n = 6) frogs. Missing data were the result of limited blood volumes, which precluded N/L or BKA analysis for some frogs. Principal components 1 and 2 collectively accounted for 77% of the observed variation in the data set (Fig. 4). Visualization of these components revealed that dying frogs, survivors and control animals represented three distinct physiological groups. Frogs surviving infection were associated with high BKA, low N/L ratios, intermediate body mass gain and high zoospore loads. In contrast, frogs dying of chytridiomycosis exhibited low BKA, high N/L ratios, low body mass gain and high zoospore loads. Control frogs were associated with high body mass gain, but substantial variation in immune function.Figure 4:

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