Larval exposure to a pyrethroid insecticide and competition for food modulate the melanisation and antibacterial responses of adult Anopheles gambiae

Abstract

the insecticides we use for agriculture and for vector control often arrive in water bodies, where mosquito larvae may be exposed to them. Not only will they then likely affect the development of the larvae, but their effects may carry over to the adults, potentially affecting their capacity at transmitting infectious diseases. Such an impact may be expected to be more severe when mosquitoes are undernourished. in this study, we investigated whether exposing larvae of the mosquito Anopheles gambiae to a sub-lethal dose of permethrin (a pyrethroid) and forcing them to compete for food would affect the immune response of the adults. We found that a low dose of permethrin increased the degree to which individually reared larvae melanised a negatively charged Sephadex bead and slowed the replication of injected Escherichia coli. However, if mosquitoes had been reared in groups of three (and thus had been forced to compete for food) permethrin had less impact on the efficacy of the immune responses. Our results show how larval stressors can affect the immune response of adults, and that the outcome of exposure to insecticides strongly depends on environmental conditions.The immune system of mosquito vectors underlies their susceptibility to parasites, and thus their ability to transmit pathogens to humans 1,2 . While the strength of their immune response has a strong genetic component 3 , it is also influenced by the environment. Adult Anopheles gambiae, for example, have a less effective melanisation response if they were undernourished as larvae 4 . Correspondingly, the ability to transmit pathogens is influenced by the environment. Examples are that vectorial competence is influenced by the bacterial microbiota the mosquitoes acquire as larvae 5 , and that the susceptibility of Aedes mosquitoes to arboviruses and of Anopheles mosquitoes to malaria parasites depend on the temperature and food conditions during larval development 6-8 .One aspect of the environment that is becoming increasingly important is the presence of insecticides. Because insecticides are used extensively in agriculture and vector control, they are often found in water of agricultural areas 9 , where mosquito larvae are exposed to them. Although their concentration is often so low that they do not kill the larvae, they affect the mosquitoes' development. In particular, their effects can carry over to adults to influence their life-history traits (reproductive success, adult longevity, sex ratio 10-13 ) and their vectorial competence for arboviruses 14,15 and malaria 16,17 .Such effects of sub-lethal doses of insecticides on vectorial competence are likely to be linked to their impact on the immune response. Indeed, exposure to insecticides affects the immune response of insects in several ways 18 : botanical insecticides 19,20 , an insect growth regulator 21 and a pyrethroid 22 decrease the activity of phenoloxidase (which is involved in the melanisation immune response) and botanical insecticides 23 , organophosphates and organochlorines 24 aff...

Consequences of larval competition and exposure to permethrin for the development of the rodent malaria Plasmodium berghei in the mosquito Anopheles gambiae

“…That, overall, competition decreased the longevity of the mosquitoes corroborates previous work [25] and may be a consequence of the reduced resource availability, leading to small females [50] and limiting mosquitoes' immune responses (e.g. [5,51]). Similarly, that permethrin exposure did not affect the longevity of individually reared mosquitoes corroborates studies that found no or negative effect of insecticide on post-infection survival following larvicidal (Bti) [19] or pyrethroid exposure [15,52].…”

“…However, in our experiment mosquitoes that were exposed both as larvae and as adults survived longer than unexposed ones, if they had been reared with competition. This suggests that the insecticide alleviate the costs of the infection, perhaps by helping mosquito immunity [5], as suggested by the results on prevalence. In individually reared mosquitoes, however, the high survival rate 22 days after the infection (c.80%) may have hidden any beneficial effect of permethrin exposure.…”

“…Alternatively, the observed effects may be due to an indirect effect of the insecticide on mosquito physiology and immunity. Insecticides can affect insect immunity in several ways (reviewed in [55]), including effects on the number of hemocytes [56], on the activity of immune enzymes [57,58], on the melanisation and antibacterial responses [5] and on oxidative stress. Indeed, pyrethroid insecticides are a major source of reactive oxygen species (ROS) in exposed organisms [3,4,59], and ROS are a common immune defense against many pathogens [60], including Plasmodium [61][62][63].…”

“…Such sublethal concentrations can increase oxidative stress [3,4], modulate the immune responses [5], and increase the activity of detoxifying enzymes [6][7][8] and the metabolic cost associated with detoxification. They can also affect the behavior of mosquitoes [9][10][11][12], in particular if the insecticide is neurotoxic.…”

Actions of camptothecin derivatives on larvae and adults of the arboviral vectorAedes aegypti

“…And whilst pyrethroid use in water sources is now prohibited because of toxicity to fish (Farag et al, 2021), pyrethroids used in agriculture are known to leach into aquatic ecosystems. Even at the low concentrations observed, early larval exposure is thought to exacerbate the development of pyrethroid resistance in adults (Churcher et al, 2016) in areas where mosquito control is needed (Diabate et al, 2002) and that such larval stressors can impact the adult immune response (Hauser and Koella, 2020).…”