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Maternal Exposure of a Beetle to Pathogens Protects Offspring against Fungal Disease.

Fisher JJ, Hajek AE - PLoS ONE (2015)

Bottom Line: Our results show that TGIP occurred and protected offspring against Metarhizium brunneum.Moreover, TGIP in response to M. brunneum occurred only after maternal exposure to living rather than dead fungus.Our findings suggest that occurrence of TGIP could be both specific and dependent on whether the pathogen was alive.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Cornell University, Ithaca, New York, United States of America.

ABSTRACT
Maternal exposure to an immune challenge can convey enhanced immunity to invertebrate offspring in the next generation. We investigated whether maternal exposure of the Asian longhorned beetle, Anoplophora glabripennis, to two species of the fungus Metarhizium or the bacterium Serratia marcescens elicited transgenerational immune priming (TGIP). We tested specificity of this protection and whether occurrence of TGIP was dependent on maternal exposure to living versus dead pathogens. Our results show that TGIP occurred and protected offspring against Metarhizium brunneum. Maternal exposure to S. marcescens provided non-specific protection to offspring against a fungal pathogen, but TGIP in response to Metarhizium only occurred when offspring were exposed to the same fungal species that was used to prime mothers. Moreover, TGIP in response to M. brunneum occurred only after maternal exposure to living rather than dead fungus. Our findings suggest that occurrence of TGIP could be both specific and dependent on whether the pathogen was alive.

No MeSH data available.


Related in: MedlinePlus

Survival curves for offspring of the S. marcescens treatment.Percentages of male and female (merged) offspring treated with M. brunneum surviving over time whose mothers were challenged with either S. marcescens or a control treatment (naive control or broth control). Different letters signify significant differences in survival curves between treatments (risk ratios, p ≤ 0.0167).
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pone.0125197.g001: Survival curves for offspring of the S. marcescens treatment.Percentages of male and female (merged) offspring treated with M. brunneum surviving over time whose mothers were challenged with either S. marcescens or a control treatment (naive control or broth control). Different letters signify significant differences in survival curves between treatments (risk ratios, p ≤ 0.0167).

Mentions: We found evidence of TGIP for offspring challenged with M. brunneum whose mothers were treated with the gram negative bacterium S. marcescens, as these offspring lived significantly longer than controls (χ22 = 23.57, p < 0.0001; risk ratios, p ≤ 0.0167, Table 1, Fig 1). Maternal exposure to S. marcescens increased offspring survival by a median of 15–16.5 d compared to controls (median days to death: S. marcescens, 42 d (95% CI: 36, 46); naive control, 25.5 d (CI: 23, 34); broth control, 27 d (CI: 19, 37)). There was no effect of sex for time to death of offspring whose mothers were either exposed to S. marcescens or received a control treatment (χ21 = 1.99, p = 0.1585). Additionally, we found evidence of immune priming for offspring challenged with M. brunneum whose mothers were treated with living M. brunneum (χ21 = 9.07, p = 0.0026, Fig 2). These beetles lived significantly longer than naive controls (median days to death: living M. brunneum, 29 d (CI: 27, 37); naive control, 25.5 d (CI: 23, 34)). There was no effect of sex for offspring whose mothers were either exposed to living M. brunneum or received the control treatment (χ21 = 0.22, p = 0.6363). Offspring challenged with M. brunneum whose mothers were injected with heat-killed M. brunneum or inoculated with living M. anisopliae did not live significantly longer than the respective controls (heat-killed M. brunneum, χ22 = 0.74, p = 0.6896, S1 Fig; living M. anisopliae, χ21 = 0.13, p = 0.7216, S2 Fig). There was no effect of sex for offspring whose mothers were exposed to heat-killed M. brunneum or offspring exposed to living M. anisopliae or their respective controls (heat-killed M. brunneum, χ21 = 0.38, p = 0.5375; living M. anisopliae, χ21 = 0.36, p = 0.5465). Interactions between sex and treatment for all models were not significant and were removed.


Maternal Exposure of a Beetle to Pathogens Protects Offspring against Fungal Disease.

Fisher JJ, Hajek AE - PLoS ONE (2015)

Survival curves for offspring of the S. marcescens treatment.Percentages of male and female (merged) offspring treated with M. brunneum surviving over time whose mothers were challenged with either S. marcescens or a control treatment (naive control or broth control). Different letters signify significant differences in survival curves between treatments (risk ratios, p ≤ 0.0167).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4418818&req=5

pone.0125197.g001: Survival curves for offspring of the S. marcescens treatment.Percentages of male and female (merged) offspring treated with M. brunneum surviving over time whose mothers were challenged with either S. marcescens or a control treatment (naive control or broth control). Different letters signify significant differences in survival curves between treatments (risk ratios, p ≤ 0.0167).
Mentions: We found evidence of TGIP for offspring challenged with M. brunneum whose mothers were treated with the gram negative bacterium S. marcescens, as these offspring lived significantly longer than controls (χ22 = 23.57, p < 0.0001; risk ratios, p ≤ 0.0167, Table 1, Fig 1). Maternal exposure to S. marcescens increased offspring survival by a median of 15–16.5 d compared to controls (median days to death: S. marcescens, 42 d (95% CI: 36, 46); naive control, 25.5 d (CI: 23, 34); broth control, 27 d (CI: 19, 37)). There was no effect of sex for time to death of offspring whose mothers were either exposed to S. marcescens or received a control treatment (χ21 = 1.99, p = 0.1585). Additionally, we found evidence of immune priming for offspring challenged with M. brunneum whose mothers were treated with living M. brunneum (χ21 = 9.07, p = 0.0026, Fig 2). These beetles lived significantly longer than naive controls (median days to death: living M. brunneum, 29 d (CI: 27, 37); naive control, 25.5 d (CI: 23, 34)). There was no effect of sex for offspring whose mothers were either exposed to living M. brunneum or received the control treatment (χ21 = 0.22, p = 0.6363). Offspring challenged with M. brunneum whose mothers were injected with heat-killed M. brunneum or inoculated with living M. anisopliae did not live significantly longer than the respective controls (heat-killed M. brunneum, χ22 = 0.74, p = 0.6896, S1 Fig; living M. anisopliae, χ21 = 0.13, p = 0.7216, S2 Fig). There was no effect of sex for offspring whose mothers were exposed to heat-killed M. brunneum or offspring exposed to living M. anisopliae or their respective controls (heat-killed M. brunneum, χ21 = 0.38, p = 0.5375; living M. anisopliae, χ21 = 0.36, p = 0.5465). Interactions between sex and treatment for all models were not significant and were removed.

Bottom Line: Our results show that TGIP occurred and protected offspring against Metarhizium brunneum.Moreover, TGIP in response to M. brunneum occurred only after maternal exposure to living rather than dead fungus.Our findings suggest that occurrence of TGIP could be both specific and dependent on whether the pathogen was alive.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Cornell University, Ithaca, New York, United States of America.

ABSTRACT
Maternal exposure to an immune challenge can convey enhanced immunity to invertebrate offspring in the next generation. We investigated whether maternal exposure of the Asian longhorned beetle, Anoplophora glabripennis, to two species of the fungus Metarhizium or the bacterium Serratia marcescens elicited transgenerational immune priming (TGIP). We tested specificity of this protection and whether occurrence of TGIP was dependent on maternal exposure to living versus dead pathogens. Our results show that TGIP occurred and protected offspring against Metarhizium brunneum. Maternal exposure to S. marcescens provided non-specific protection to offspring against a fungal pathogen, but TGIP in response to Metarhizium only occurred when offspring were exposed to the same fungal species that was used to prime mothers. Moreover, TGIP in response to M. brunneum occurred only after maternal exposure to living rather than dead fungus. Our findings suggest that occurrence of TGIP could be both specific and dependent on whether the pathogen was alive.

No MeSH data available.


Related in: MedlinePlus