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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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Experimental design of a) experiment 1 and b) experiment 2.
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Fig1: Experimental design of a) experiment 1 and b) experiment 2.

Mentions: Two experiments were carried out (Figure 1). In the first experiment, F0 females received one blood meal (either I or NI) and were then placed in individual cups. Two days afterwards an oviposition site (wet filter paper) was added at the cup bottoms. On day 3 post-blood meal, eggs were retrieved from the cups and transferred to plastic cups filled with water. Larvae were fed ad libitum Tetramin® food. Upon emergence, F1 adult mosquitoes belonging to the same brood were transferred to paper cups and provided with 2.5% glucose solution. Three- to five-day-old offspring females of both maternal groups (I and NI) that developed at the same rate (i.e., same age structure) received an infectious blood meal from the same gametocyte carrier on the same day. Fully fed females then returned to their assigned cups. They were dissected eight days later to estimate their resistance to P. falciparum. Specifically, infection rate and intensity were quantified. Infection rate is the proportion of infected females, and relates to the mosquito’s ability to prevent infection (qualitative resistance). Infection intensity is the number of oocysts found in the gut of infected females and relates to their ability to limit parasite development (quantitative resistance). These traits were also measured in F0 females (Additional file 1). This experiment used a total of 377 F1 females (from 27 infected and 31 control mothers).Figure 1


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

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

Experimental design of a) experiment 1 and b) experiment 2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4255934&req=5

Fig1: Experimental design of a) experiment 1 and b) experiment 2.
Mentions: Two experiments were carried out (Figure 1). In the first experiment, F0 females received one blood meal (either I or NI) and were then placed in individual cups. Two days afterwards an oviposition site (wet filter paper) was added at the cup bottoms. On day 3 post-blood meal, eggs were retrieved from the cups and transferred to plastic cups filled with water. Larvae were fed ad libitum Tetramin® food. Upon emergence, F1 adult mosquitoes belonging to the same brood were transferred to paper cups and provided with 2.5% glucose solution. Three- to five-day-old offspring females of both maternal groups (I and NI) that developed at the same rate (i.e., same age structure) received an infectious blood meal from the same gametocyte carrier on the same day. Fully fed females then returned to their assigned cups. They were dissected eight days later to estimate their resistance to P. falciparum. Specifically, infection rate and intensity were quantified. Infection rate is the proportion of infected females, and relates to the mosquito’s ability to prevent infection (qualitative resistance). Infection intensity is the number of oocysts found in the gut of infected females and relates to their ability to limit parasite development (quantitative resistance). These traits were also measured in F0 females (Additional file 1). This experiment used a total of 377 F1 females (from 27 infected and 31 control mothers).Figure 1

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