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Parental and offspring larval diets interact to influence life-history traits and infection with dengue virus in Aedes aegypti.

ABSTRACT: The environmental conditions experienced by parents can influence offspring phenotype along with the conditions experienced by offspring. These parental effects are clear in organisms that display parental care and are less clear in other organisms. Here, we consider effects of parental and offspring larval nutrition on offspring development time, survivorship and infection with dengue virus in Aedes aegypti, the mosquito vector of dengue, chikungunya, yellow fever and Zika. Parents were raised on either high or low larval detritus inputs with subsequent offspring being divided into two groups, one receiving high nutrients and the other low. Low nutrient females from low nutrient parents (LL) developed significantly slower than those from high nutrient parents (HL). Females from all parent by offspring nutrient treatment groups were equally likely to become infected with dengue virus at 24?h, 3 days and 14 days. After 14 days, high nutrient females from low nutrient parents (LH) had 11 times higher viral titres and more disseminated infections than high nutrient females from high nutrient parents (HH). These results suggest that carry-over environmental stress from the parental generation can influence life histories and arbovirus infection in Ae. aegypti females. We found males to be robust to the life-history parameters measured, suggesting sex-specific differences which may relate to their lower nutrient requirements for metamorphosis.

SUBMITTER: Zirbel K

PROVIDER: S-EPMC6083674 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Parental and offspring larval diets interact to influence life-history traits and infection with dengue virus in <i>Aedes aegypti</i>.

Zirbel Kylie K Eastmond Bradley B Alto Barry W BW

Royal Society open science 20180718 7

The environmental conditions experienced by parents can influence offspring phenotype along with the conditions experienced by offspring. These parental effects are clear in organisms that display parental care and are less clear in other organisms. Here, we consider effects of parental and offspring larval nutrition on offspring development time, survivorship and infection with dengue virus in <i>Aedes aegypti</i>, the mosquito vector of dengue, chikungunya, yellow fever and Zika. Parents were ...[more]

PMID: 30109101

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Project description:Effectively controlling vector mosquito populations while avoiding the development of resistance remains a prevalent and increasing obstacle to integrated vector management. Although, metallic nanoparticles have previously shown promise in controlling larval populations via mechanisms which are less likely to spur resistance, the impacts of such particles on life history traits and fecundity of mosquitoes are understudied. Herein, we investigate the chemically well-defined cerium oxide nanoparticles (CNPs) and silver-doped nanoceria (AgCNPs) for larvicidal potential and effects on life history traits and fecundity of Aedes (Ae.) aegypti mosquitoes. When 3rd instar larvae were exposed to nanoceria in absence of larval food, the mortality count disclosed significant activity of AgCNPs over CNPs (57.8±3.68% and 17.2±2.81% lethality, respectively) and a comparable activity to Ag+ controls (62.8±3.60% lethality). The surviving larvae showed altered life history traits (e.g., reduced egg hatch proportion and varied sex ratios), indicating activities of these nanoceria beyond just that of a larvicide. In a separate set of experiments, impacts on oocyte growth and egg generation resulting from nanoceria-laced blood meals were studied using confocal fluorescence microscopy revealing oocytes growth-arrest at 16-24h after feeding with AgCNP-blood meals in some mosquitoes, thereby significantly reducing average egg clutch. AgCNPs caused ~60% mortality in 3rd instar larvae when larval food was absent, while CNPs yielded only ~20% mortality which contrasts with a previous report on green-synthesized nanoceria and highlights the level of detail required to accurately report and interpret such studies. Additionally, AgCNPs are estimated to contain much less silver (0.22 parts per billion, ppb) than the amount of Ag+ needed to achieve comparable larvicidal activity (2.7 parts per million, ppm), potentially making these nanoceria ecofriendly. Finally, this work is the first study to demonstrate the until-now-unappreciated impacts of nanoceria on life history traits and interference with mosquito egg development.

Project description:BackgroundCurrent Aedes aegypti larval control methods are often insufficient for preventing dengue epidemics. To improve control efficiency and cost-effectiveness, some advocate eliminating or treating only highly productive containers. The population-level outcome of this strategy, however, will depend on details of Ae. aegypti oviposition behavior.Methodology/principal findingsWe simultaneously monitored female oviposition and juvenile development in 80 experimental containers located across 20 houses in Iquitos, Peru, to test the hypothesis that Ae. aegypti oviposit preferentially in sites with the greatest potential for maximizing offspring fitness. Females consistently laid more eggs in large vs. small containers (??=?9.18, p<0.001), and in unmanaged vs. manually filled containers (??=?5.33, p<0.001). Using microsatellites to track the development of immature Ae. aegypti, we found a negative correlation between oviposition preference and pupation probability (??=?-3.37, p<0.001). Body size of emerging adults was also negatively associated with the preferred oviposition site characteristics of large size (females: ??=?-0.19, p<0.001; males: ??=?-0.11, p?=?0.002) and non-management (females: ??=?-0.17, p<0.001; males: ??=?-0.11, p<0.001). Inside a semi-field enclosure, we simulated a container elimination campaign targeting the most productive oviposition sites. Compared to the two post-intervention trials, egg batches were more clumped during the first pre-intervention trial (??=?-0.17, P<0.001), but not the second (??=?0.01, p?=?0.900). Overall, when preferred containers were unavailable, the probability that any given container received eggs increased (??=?1.36, p<0.001).Conclusions/significanceAe. aegypti oviposition site choice can contribute to population regulation by limiting the production and size of adults. Targeted larval control strategies may unintentionally lead to dispersion of eggs among suitable, but previously unoccupied or under-utilized containers. We recommend integrating targeted larval control measures with other strategies that leverage selective oviposition behavior, such as luring ovipositing females to gravid traps or egg sinks.

Project description:BACKGROUND:Producing high quality sterile males is vital in Aedes aegypti rear-and-release birth control strategies. Larval diets, rearing temperatures, and their interactions determine the accumulation rates of essential nutrients in larvae, but these factors have been understudied in relation to mass-rearing techniques for producing eminent males. METHODS:We compared the effects of two larval diets, a cereal-legume-based diet (Khan's diet) and a standard larval diet developed in the FAO/IAEA Insect Pest Control Laboratory (IAEA 2 diet). Diets were tested at selected temperatures for both larval and male adult life history traits, adult extreme temperature tolerance, and mating capacity relative to energy reserves of reared male adult Ae. aegypti. RESULTS:Khan's diet resulted in shorter immature development time at each test temperature (except for 25 °C) than an IAEA 2 diet. Larvae reared at 28 °C and 32 °C with Khan's diet demonstrated low pupation rates (c.80%). We accounted for these phenomena as secondary sex ratio manipulation, because a higher proportion of male adults emerged at 28 °C and 32 °C than that for the IAEA 2 diet. In general, the pupal development time shortened as temperature increased, resulting in higher teneral energy reserves in male mosquitoes. High energy reserves allowed male mosquitoes reared with Khan's diet to have higher adult longevity (5-6 days longer when sugar-fed and 2-3 days longer when water-fed) and tolerance of heat stress than those fed on the IAEA 2 diet. The IAEA 2 diet produced larger male mosquitoes than Khan's diet did: mosquitoes fed on Khan's diet were 1.03-1.05 times smaller than those fed on the IAEA 2 diet at 28 °C and 32 °C. No evidence indicated reduced mating capacity for small mosquitoes fed on Khan's diet. CONCLUSIONS:Larvae reared at 28 °C and 32 °C with Khan's diet were characterized by shorter immature development time compared with those fed on the IAEA 2 diet. Adult mosquitoes produced from that larval rearing condition exhibited a significant male bias, long lifespan, and better endurance against extreme temperatures relative to energy reserves. Thus, the larval diet at rearing temperature of 28 °C and 32 °C optimized rearing techniques for the sterile insect programmes. However, mating competitiveness and flight performance of adult males require further investigation.

Dataset Information

Parental and offspring larval diets interact to influence life-history traits and infection with dengue virus in Aedes aegypti.

Publications

Parental and offspring larval diets interact to influence life-history traits and infection with dengue virus in <i>Aedes aegypti</i>.

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