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A heavy legacy: offspring of malaria-infected mosquitoes show reduced disease resistance.

Vantaux A, Dabiré KR, Cohuet A, Lefèvre T - Malar. J. (2014)

Bottom Line: However, maternal disease exposure altered offspring quantitative resistance, measured as the ability to limit parasite development, with mosquitoes of infected mothers suffering slightly increased parasite intensity compared to controls.Plasmodium falciparum infection in An. coluzzii can have trans-generational costs, lowering quantitative resistance in offspring of infected mothers.Malaria-exposed mosquitoes might heavily invest in immune defences and thereby produce lower quality offspring that are poorly resistant.

View Article: PubMed Central - PubMed

Affiliation: UMR MIVEGEC (IRD 224 - CNRS 5290 - UM1 - UM2), 911 Avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France. amelie.vantaux@gmail.com.

ABSTRACT

Background: Trans-generational effects of immune stimulation may have either adaptive (trans-generational immune priming) or non-adaptive (fitness costs) effects on offspring ability to fight pathogens.

Methods: Anopheles coluzzii and its natural malaria parasite Plasmodium falciparum were used to test how maternal parasite infection affected offspring resistance to the same parasite species.

Results: Daughters of exposed mothers had similar qualitative resistance, as measured by their ability to prevent infection, relative to those of control mothers. However, maternal disease exposure altered offspring quantitative resistance, measured as the ability to limit parasite development, with mosquitoes of infected mothers suffering slightly increased parasite intensity compared to controls. In addition, quantitative resistance was minimal in offspring of highly infected mothers, and in offspring issued from eggs produced during the early infection phase.

Conclusions: Plasmodium falciparum infection in An. coluzzii can have trans-generational costs, lowering quantitative resistance in offspring of infected mothers. Malaria-exposed mosquitoes might heavily invest in immune defences and thereby produce lower quality offspring that are poorly resistant.

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Trans-generational effects of infection on offspring quantitative resistance (a) in experiment 1; (b) in experiment 2; (c) Positive relationship between infection intensity in F1 and F0 mosquitoes. The grey area represents the 95% confidence interval. The quadratic term of mother’s infection intensity was not a good predictor (Additional file 6). BM: blood meal, I: infectious, NI: non-infectious. Bars with different letters are significantly different (post-hoc Bonferroni-corrected comparisons).
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Fig2: Trans-generational effects of infection on offspring quantitative resistance (a) in experiment 1; (b) in experiment 2; (c) Positive relationship between infection intensity in F1 and F0 mosquitoes. The grey area represents the 95% confidence interval. The quadratic term of mother’s infection intensity was not a good predictor (Additional file 6). BM: blood meal, I: infectious, NI: non-infectious. Bars with different letters are significantly different (post-hoc Bonferroni-corrected comparisons).

Mentions: Maternal exposure was marginally related to quantitative resistance in experiment 1 (72 ± 6 oocysts vs 62 ± 4, ΔAIC = 1.6, ΔAICc = 1.7, Figure 2a, Additional file 4), while there was a positive relationship between mosquito size and quantitative resistance (ΔAIC = 4.6, ΔAICc = 4.5). However, neither maternal exposure nor maternal body size influenced offspring size (ΔAIC = 3.3 and 3.8, respectively, ΔAICc = 3.4 and 3.9 respectively, Additional file 5). In experiment 2, maternal exposure was also marginally associated with quantitative resistance with first-batch offspring of exposed mothers harbouring slightly more parasites than those of control mothers (19 ± 2 in I-1 vs 15 ± 2 in NI-1, ΔAIC = 1.4, ΔAICc = 1.2, Figure 2b, Additional file 4). However, when first-batch offspring of experiment one and two were pooled together, maternal parasite exposure significantly influenced offspring quantitative resistance (52 ± 4 vs 49 ± 3: ΔAIC = 2.3, ΔAICc = 2.3, Additional file 4). In addition, infection intensity in F0 mosquitoes was associated with intensity in offspring (ΔAIC = 2.1, ΔAICc = 2; Figure 2c, Additional file 6). Among second-batch offspring, the best model explaining variation in oocyst number also included maternal treatment (ΔAIC = 3, ΔAICc = 2.8, Figure 2b, Additional file 4). Infection intensity ranged from 15 oocysts ±2 in I-NI-2, to 18 ± 2 in I-I-2 and 26 ± 2 in NI-I-2 offspring. Finally, data from experiment 2, altogether (replicate 1 and 2, egg-lay 1 and 2), indicated that recent maternal exposure to P. falciparum strongly affected offspring quantitative resistance (ΔAIC = 5.6, ΔAICc = 5.4, Additional file 7) such that highest intensities were observed in offspring arising from eggs whose development was initiated by an infectious blood meal (i.e., I-1, I-I-2, NI-I-2, Figure 2b).Figure 2


A heavy legacy: offspring of malaria-infected mosquitoes show reduced disease resistance.

Vantaux A, Dabiré KR, Cohuet A, Lefèvre T - Malar. J. (2014)

Trans-generational effects of infection on offspring quantitative resistance (a) in experiment 1; (b) in experiment 2; (c) Positive relationship between infection intensity in F1 and F0 mosquitoes. The grey area represents the 95% confidence interval. The quadratic term of mother’s infection intensity was not a good predictor (Additional file 6). BM: blood meal, I: infectious, NI: non-infectious. Bars with different letters are significantly different (post-hoc Bonferroni-corrected comparisons).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4255934&req=5

Fig2: Trans-generational effects of infection on offspring quantitative resistance (a) in experiment 1; (b) in experiment 2; (c) Positive relationship between infection intensity in F1 and F0 mosquitoes. The grey area represents the 95% confidence interval. The quadratic term of mother’s infection intensity was not a good predictor (Additional file 6). BM: blood meal, I: infectious, NI: non-infectious. Bars with different letters are significantly different (post-hoc Bonferroni-corrected comparisons).
Mentions: Maternal exposure was marginally related to quantitative resistance in experiment 1 (72 ± 6 oocysts vs 62 ± 4, ΔAIC = 1.6, ΔAICc = 1.7, Figure 2a, Additional file 4), while there was a positive relationship between mosquito size and quantitative resistance (ΔAIC = 4.6, ΔAICc = 4.5). However, neither maternal exposure nor maternal body size influenced offspring size (ΔAIC = 3.3 and 3.8, respectively, ΔAICc = 3.4 and 3.9 respectively, Additional file 5). In experiment 2, maternal exposure was also marginally associated with quantitative resistance with first-batch offspring of exposed mothers harbouring slightly more parasites than those of control mothers (19 ± 2 in I-1 vs 15 ± 2 in NI-1, ΔAIC = 1.4, ΔAICc = 1.2, Figure 2b, Additional file 4). However, when first-batch offspring of experiment one and two were pooled together, maternal parasite exposure significantly influenced offspring quantitative resistance (52 ± 4 vs 49 ± 3: ΔAIC = 2.3, ΔAICc = 2.3, Additional file 4). In addition, infection intensity in F0 mosquitoes was associated with intensity in offspring (ΔAIC = 2.1, ΔAICc = 2; Figure 2c, Additional file 6). Among second-batch offspring, the best model explaining variation in oocyst number also included maternal treatment (ΔAIC = 3, ΔAICc = 2.8, Figure 2b, Additional file 4). Infection intensity ranged from 15 oocysts ±2 in I-NI-2, to 18 ± 2 in I-I-2 and 26 ± 2 in NI-I-2 offspring. Finally, data from experiment 2, altogether (replicate 1 and 2, egg-lay 1 and 2), indicated that recent maternal exposure to P. falciparum strongly affected offspring quantitative resistance (ΔAIC = 5.6, ΔAICc = 5.4, Additional file 7) such that highest intensities were observed in offspring arising from eggs whose development was initiated by an infectious blood meal (i.e., I-1, I-I-2, NI-I-2, Figure 2b).Figure 2

Bottom Line: However, maternal disease exposure altered offspring quantitative resistance, measured as the ability to limit parasite development, with mosquitoes of infected mothers suffering slightly increased parasite intensity compared to controls.Plasmodium falciparum infection in An. coluzzii can have trans-generational costs, lowering quantitative resistance in offspring of infected mothers.Malaria-exposed mosquitoes might heavily invest in immune defences and thereby produce lower quality offspring that are poorly resistant.

View Article: PubMed Central - PubMed

Affiliation: UMR MIVEGEC (IRD 224 - CNRS 5290 - UM1 - UM2), 911 Avenue Agropolis, BP 64501, 34394 Montpellier Cedex 5, France. amelie.vantaux@gmail.com.

ABSTRACT

Background: Trans-generational effects of immune stimulation may have either adaptive (trans-generational immune priming) or non-adaptive (fitness costs) effects on offspring ability to fight pathogens.

Methods: Anopheles coluzzii and its natural malaria parasite Plasmodium falciparum were used to test how maternal parasite infection affected offspring resistance to the same parasite species.

Results: Daughters of exposed mothers had similar qualitative resistance, as measured by their ability to prevent infection, relative to those of control mothers. However, maternal disease exposure altered offspring quantitative resistance, measured as the ability to limit parasite development, with mosquitoes of infected mothers suffering slightly increased parasite intensity compared to controls. In addition, quantitative resistance was minimal in offspring of highly infected mothers, and in offspring issued from eggs produced during the early infection phase.

Conclusions: Plasmodium falciparum infection in An. coluzzii can have trans-generational costs, lowering quantitative resistance in offspring of infected mothers. Malaria-exposed mosquitoes might heavily invest in immune defences and thereby produce lower quality offspring that are poorly resistant.

Show MeSH
Related in: MedlinePlus