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Article ; Online: Resource availability for the mosquito Aedes aegypti affects the transmission mode evolution of a microsporidian parasite

Zilio, Giacomo / Kaltz, Oliver / Koella, Jacob C.

Evol Ecol. 2023 Feb., v. 37, no. 1 p.31-51

2023

Abstract: Ecological conditions may greatly affect the relative importance of vertical and horizontal transmission, in particular for parasites with a mixed mode of transmission. Resource availability is one important environmental factor, affecting host growth ... ...

Abstract	Ecological conditions may greatly affect the relative importance of vertical and horizontal transmission, in particular for parasites with a mixed mode of transmission. Resource availability is one important environmental factor, affecting host growth and fecundity, but also the parasite’s own development. The consequences for the potential of vertical and horizontal transmission and for the evolution of transmission mode are largely unknown. We let the mixed-mode microsporidian parasite Edhazardia aedis evolve on its mosquito host Aedes aegypti under high-food or low-food conditions, representing permissive and restricted conditions. These alter the timing of development of infected larvae and thereby the probabilities for the parasites to enter the vertical or horizontal transmission pathways. After 10 generations, evolved parasites were assayed under the two food levels. There was an ecological trade-off between transmission modes, mediated by nutrient effects on host development, resulting in a higher vertical transmission (VT) potential under high-food and a higher horizontal transmission (HT) potential under low-food test conditions. Evolution under high food increased the VT potential of the parasite, particularly if it was tested at low food. This involved higher probability of carrying binucleate spores for the emerging females, greater fecundity and a longer life compared to parasites that were tested in the same conditions but had evolved under low food. The changes are related to the developmental regulation and switch in the production of two spore types, affecting investment in VT or HT. In contrast, the HT potential remained relatively unaffected by the parasite’s evolutionary history, suggesting that, within our experiential design, the VT mode evolved independently of the HT mode. Our work illustrates the possible links between resource availability, within-host developmental processes and the evolution of parasite transmission investment. Future work, theoretical and experimental, should scale up from within-host to between-host levels, including eco-evolutionary and epidemiological dynamics.
Keywords	Aedes aegypti ; Edhazardia aedis ; environmental factors ; evolution ; fecundity ; parasites ; probability ; spores
Language	English
Dates of publication	2023-02
Size	p. 31-51.
Publishing place	Springer International Publishing
Document type	Article ; Online
ZDB-ID	15919-0
ISSN	1573-8477 ; 0269-7653
ISSN (online)	1573-8477
ISSN	0269-7653
DOI	10.1007/s10682-022-10184-7
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Article ; Online: Unexpected behavioural adaptation of yellow fever mosquitoes in response to high temperatures.

Hug, David O H / Kropf, Alida / Amann, Marine O / Koella, Jacob C / Verhulst, Niels O

Scientific reports

2024 Volume 14, Issue 1, Page(s) 3659

Abstract: Temperature is a major ecological driver of mosquito-borne diseases as it influences the life-history of both the mosquito and the pathogen harboured within it. Understanding the mosquitoes' thermal biology is essential to inform risk prediction models ... ...

Abstract	Temperature is a major ecological driver of mosquito-borne diseases as it influences the life-history of both the mosquito and the pathogen harboured within it. Understanding the mosquitoes' thermal biology is essential to inform risk prediction models of such diseases. Mosquitoes can respond to temperatures by microhabitat selection through thermal preference. However, it has not yet been considered that mosquitoes are likely to adapt to changing temperatures, for example during climate change, and alter their preference over evolutionary time. We investigated this by rearing six cohorts of the yellow fever mosquito Aedes aegypti at two temperatures (24 °C, 30 °C) for 20 generations and used these cohorts to explicitly separate the effects of long-term evolution and within-generation acclimation on their thermal preferences in a thermal gradient of 20-35 °C. We found that warm-evolved mosquitoes spent 31.5% less time at high temperatures, which affects their efficiency as a vector. This study reveals the complex interplay of experimental evolution, rearing temperatures, and thermal preference in Ae. aegypti mosquitoes. It highlights the significance of incorporating mosquito microhabitat selection in disease transmission models, especially in the context of climate change.
MeSH term(s)	Animals ; Yellow Fever ; Temperature ; Mosquito Vectors ; Aedes/physiology ; Climate Change
Language	English
Publishing date	2024-02-13
Publishing country	England
Document type	Journal Article
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-024-54374-5
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Article ; Online: Larval exposure to a pyrethroid insecticide and competition for food modulate the melanisation and antibacterial responses of adult Anopheles gambiae.

Hauser, Gaël / Koella, Jacob C

Scientific reports

2020 Volume 10, Issue 1, Page(s) 1364

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, ...

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.
MeSH term(s)	Animals ; Anopheles/immunology ; Anopheles/microbiology ; Escherichia coli/immunology ; Feeding Behavior/drug effects ; Food ; Insecticides/pharmacology ; Larva/immunology ; Larva/microbiology ; Mosquito Vectors/immunology ; Mosquito Vectors/microbiology ; Permethrin/pharmacology
Chemical Substances	Insecticides ; Permethrin (509F88P9SZ)
Language	English
Publishing date	2020-01-28
Publishing country	England
Document type	Journal Article
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-020-58415-7
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Article ; Online: Sequential co-infections drive parasite competition and the outcome of infection.

Zilio, Giacomo / Koella, Jacob C

The Journal of animal ecology

2020 Volume 89, Issue 10, Page(s) 2367–2377

Abstract: Co-infections by multiple parasites are common in natural populations. Some of these are likely to be the result of sequential rather than simultaneous infections. The timing of the co-infections may affect their competitive interactions, thereby ... ...

Abstract	Co-infections by multiple parasites are common in natural populations. Some of these are likely to be the result of sequential rather than simultaneous infections. The timing of the co-infections may affect their competitive interactions, thereby influencing the success of the parasites and their impact on the host. This may have important consequence for epidemiological and eco-evolutionary dynamics. We examined in two ecological conditions the effect of sequential co-infection on the outcome of infection by two microsporidians, Vavraia culicis and Edhazardia aedis, that infect the mosquito Aedes aegypti. The two parasites have different transmission strategies: V. culicis is transmitted horizontally either among larvae or from adults to larvae, while E. aedis can be transmitted horizontally among larvae or vertically from females to their eggs. We investigated how the timing and order of the co-infection and how the host's food availability affected the parasite's transmission potential (the percentage of individuals that harboured transmissible spores) and the host's juvenile survival, its age at emergence and its longevity. The outcome of co-infection was strongly affected by the order at which the parasites arrived. In co-infections, V. culicis had greater horizontal transmission if it arrived early, whereas the transmission potential of E. aedis, either vertical or horizontal, was not affected by the competitor V. culicis. The availability of food determined the duration of infection leading to variation in mortality and in the transmission potential. For both parasites low food decreased juvenile survival, delayed emergence to adulthood and increased horizontal transmission potential. High food increased juvenile survival and the probability of emergence with higher vertical transmission for E. aedis. Overall, our results suggest that early infection favours transmission and that (a) V. culicis plastically responded to co-infection, (b) E. aedis was not affected by co-infection but it was more susceptible to factors extending or decreasing the time it spent in the host (time of infection and food). Our results emphasize the complexity of the impact of co-infection on host-parasite interactions. In particular, the timing and order of sequential co-infections can result in different within-host dynamics and modify infection outcomes.
MeSH term(s)	Animals ; Coinfection/veterinary ; Female ; Host-Parasite Interactions ; Microsporidia ; Parasites
Language	English
Publishing date	2020-08-10
Publishing country	England
Document type	Journal Article
ZDB-ID	3024-7
ISSN	1365-2656 ; 0021-8790
ISSN (online)	1365-2656
ISSN	0021-8790
DOI	10.1111/1365-2656.13302
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Article: Sequential co‐infections drive parasite competition and the outcome of infection

Zilio, Giacomo / Koella, Jacob C

journal of animal ecology. 2020 Oct., v. 89, no. 10

2020

Abstract: Co‐infections by multiple parasites are common in natural populations. Some of these are likely to be the result of sequential rather than simultaneous infections. The timing of the co‐infections may affect their competitive interactions, thereby ... ...

Abstract	Co‐infections by multiple parasites are common in natural populations. Some of these are likely to be the result of sequential rather than simultaneous infections. The timing of the co‐infections may affect their competitive interactions, thereby influencing the success of the parasites and their impact on the host. This may have important consequence for epidemiological and eco‐evolutionary dynamics. We examined in two ecological conditions the effect of sequential co‐infection on the outcome of infection by two microsporidians, Vavraia culicis and Edhazardia aedis, that infect the mosquito Aedes aegypti. The two parasites have different transmission strategies: V. culicis is transmitted horizontally either among larvae or from adults to larvae, while E. aedis can be transmitted horizontally among larvae or vertically from females to their eggs. We investigated how the timing and order of the co‐infection and how the host's food availability affected the parasite's transmission potential (the percentage of individuals that harboured transmissible spores) and the host's juvenile survival, its age at emergence and its longevity. The outcome of co‐infection was strongly affected by the order at which the parasites arrived. In co‐infections, V. culicis had greater horizontal transmission if it arrived early, whereas the transmission potential of E. aedis, either vertical or horizontal, was not affected by the competitor V. culicis. The availability of food determined the duration of infection leading to variation in mortality and in the transmission potential. For both parasites low food decreased juvenile survival, delayed emergence to adulthood and increased horizontal transmission potential. High food increased juvenile survival and the probability of emergence with higher vertical transmission for E. aedis. Overall, our results suggest that early infection favours transmission and that (a) V. culicis plastically responded to co‐infection, (b) E. aedis was not affected by co‐infection but it was more susceptible to factors extending or decreasing the time it spent in the host (time of infection and food). Our results emphasize the complexity of the impact of co‐infection on host–parasite interactions. In particular, the timing and order of sequential co‐infections can result in different within‐host dynamics and modify infection outcomes.
Keywords	Aedes aegypti ; Edhazardia aedis ; Vavraia culicis ; adulthood ; animal ecology ; food availability ; juveniles ; longevity ; mixed infection ; mortality ; parasites ; probability
Language	English
Dates of publication	2020-10
Size	p. 2367-2377.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	NAL-AP-2-clean ; JOURNAL ARTICLE
ZDB-ID	3024-7
ISSN	1365-2656 ; 0021-8790
ISSN (online)	1365-2656
ISSN	0021-8790
DOI	10.1111/1365-2656.13302
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Article ; Online: Use of novel lab assays to examine the effect of pyrethroid-treated bed nets on blood-feeding success and longevity of highly insecticide-resistant Anopheles gambiae s.l. mosquitoes.

Barreaux, Priscille / Koella, Jacob C / N'Guessan, Raphael / Thomas, Matthew B

Parasites & vectors

2022 Volume 15, Issue 1, Page(s) 111

Abstract: Background: There is a pressing need to improve understanding of how insecticide resistance affects the functional performance of insecticide-treated nets (ITNs). Standard WHO insecticide resistance monitoring assays are designed for resistance ... ...

Abstract	Background: There is a pressing need to improve understanding of how insecticide resistance affects the functional performance of insecticide-treated nets (ITNs). Standard WHO insecticide resistance monitoring assays are designed for resistance surveillance and do not necessarily provide insight into how different frequencies, mechanisms or intensities of resistance affect the ability of ITNs to reduce malaria transmission. Methods: The current study presents some novel laboratory-based assays that attempt to better simulate realistic exposure of mosquitoes to ITNs and to quantify impact of exposure not only on instantaneous mortality, but also on blood-feeding and longevity, two traits that are central to transmission. The assays evaluated the performance of a standard ITN (Permanet® 2.0; Vestergaard Frandsen), a 'next generation' combination ITN with a resistance-breaking synergist (Permanet® 3.0) and an untreated net (UTN), against field-derived Anopheles gambiae sensu lato mosquitoes from Côte d'Ivoire exhibiting a 1500-fold increase in pyrethroid resistance relative to a standard susceptible strain. Results: The study revealed that the standard ITN induced negligible instantaneous mortality against the resistant mosquitoes, whereas the resistance-breaking net caused high mortality and a reduction in blood-feeding. However, both ITNs still impacted long-term survival relative to the UTN. The impact on longevity depended on feeding status, with blood-fed mosquitoes living longer than unfed mosquitoes following ITN exposure. Exposure to both ITNs also reduced the blood-feeding success, the time spent on the net and blood-feeding duration, relative to the untreated net. Conclusion: Although a standard ITN did not have as substantial instantaneous impact as the resistance-breaking net, it still had significant impacts on traits important for transmission. These results highlight the benefit of improved bioefficacy assays that allow for realistic exposure and consider sub- or pre-lethal effects to help assess the functional significance of insecticide resistance.
MeSH term(s)	Animals ; Anopheles ; Insecticide Resistance ; Insecticides/pharmacology ; Mosquito Control/methods ; Pyrethrins/pharmacology
Chemical Substances	Insecticides ; Pyrethrins
Language	English
Publishing date	2022-03-28
Publishing country	England
Document type	Journal Article
ZDB-ID	2409480-8
ISSN	1756-3305 ; 1756-3305
ISSN (online)	1756-3305
ISSN	1756-3305
DOI	10.1186/s13071-022-05220-y
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Article ; Online: Exploring artificial habitat fragmentation to control invasion by infectious wildlife diseases.

Bozzuto, Claudio / Canessa, Stefano / Koella, Jacob C

Theoretical population biology

2021 Volume 141, Page(s) 14–23

Abstract: One way to reduce the impacts of invading wildlife diseases is setting up fences that would reduce the spread of pathogens by limiting connectivity, similarly to exclusion fences that are commonly used to conserve threatened species against invasive ... ...

Abstract	One way to reduce the impacts of invading wildlife diseases is setting up fences that would reduce the spread of pathogens by limiting connectivity, similarly to exclusion fences that are commonly used to conserve threatened species against invasive predators. One of the problems with fences is that, while they may have the short-term benefit of impeding the spread of disease, this benefit may be offset by potential long-term ecological costs of fragmentation by fencing. However, managers facing situations where a pathogen has been detected near the habitat of a (highly) vulnerable species may be willing to explore such a trade-off. To aid such exploration quantitatively, we present a series of models trading off the benefits of fragmentation (potential reduction of disease impacts on susceptible individuals) against its costs (both financial and ecological, i.e. reduced viability in the patches created by fragmentation), and exploring the effects of fragmentation on non-target species richness. For all model variants we derive the optimal number of artificial patches. We show that pre-emptive disease fences may have benefits when the risk of disease exceeds the impacts of fragmentation, when fence failure rates are lower than a specific threshold, and when sufficient resources are available to implement optimal solutions. A useful step to initiate planning is to obtain information about the expected number of initial infection events and on the host's extinction threshold with respect to the focal habitat and management duration. Our approach can assist managers to identify whether the trade-offs support the decision to fence and how intensive fragmentation should be.
MeSH term(s)	Animals ; Animals, Wild ; Conservation of Natural Resources ; Ecosystem ; Humans
Language	English
Publishing date	2021-06-15
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3948-2
ISSN	1096-0325 ; 0040-5809
ISSN (online)	1096-0325
ISSN	0040-5809
DOI	10.1016/j.tpb.2021.06.001
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Article ; Online: Parasite evolution in an age-structured population.

Hamley, Jonathan I D / Koella, Jacob C

Journal of theoretical biology

2021 Volume 527, Page(s) 110732

Abstract: Although mortality increases with age in most organisms, senescence is missing from models of parasite evolution. Since virulence evolves according to the host's mortality, and since virulence influences the intensity of transmission, which determines ... ...

Abstract	Although mortality increases with age in most organisms, senescence is missing from models of parasite evolution. Since virulence evolves according to the host's mortality, and since virulence influences the intensity of transmission, which determines the average age at infection and thus the mortality rate of a senescing host, we expected that epi-evolutionary feedbacks would underlie the evolution of virulence in a population of senescing hosts. We tested this idea by extending an age-structured model of epidemiological dynamics with the parasite's evolution. A straightforward prediction of our model is that stronger senescence forces the evolution of higher virulence. However, the model also reveals that the evolved virulence depends on the average age at infection, giving an evolutionary feedback with the epidemiological situation, a prediction not found when assuming a constant mortality rate with age. Additionally, and in contrast to most models of parasite evolution, we found that the virulence at the evolutionary equilibrium is influenced by whether the force of infection depends on the density or on the frequency of infected hosts, due to changes in the average age at infection. Our findings suggest that ignoring age-specific effects, and in particular senescence, can give misleading predictions about parasite evolution.
MeSH term(s)	Animals ; Biological Evolution ; Host-Parasite Interactions ; Models, Biological ; Parasites/genetics ; Virulence
Language	English
Publishing date	2021-04-27
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2972-5
ISSN	1095-8541 ; 0022-5193
ISSN (online)	1095-8541
ISSN	0022-5193
DOI	10.1016/j.jtbi.2021.110732
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Article: Use of novel lab assays to examine the effect of pyrethroid-treated bed nets on blood-feeding success and longevity of highly insecticide-resistant Anopheles gambiae s.l. mosquitoes

Barreaux, Priscille / Koella, Jacob C. / N’Guessan, Raphael / Thomas, Matthew B.

Parasites & vectors. 2022 Dec., v. 15, no. 1

2022

Abstract: BACKGROUND: There is a pressing need to improve understanding of how insecticide resistance affects the functional performance of insecticide-treated nets (ITNs). Standard WHO insecticide resistance monitoring assays are designed for resistance ... ...

Abstract	BACKGROUND: There is a pressing need to improve understanding of how insecticide resistance affects the functional performance of insecticide-treated nets (ITNs). Standard WHO insecticide resistance monitoring assays are designed for resistance surveillance and do not necessarily provide insight into how different frequencies, mechanisms or intensities of resistance affect the ability of ITNs to reduce malaria transmission. METHODS: The current study presents some novel laboratory-based assays that attempt to better simulate realistic exposure of mosquitoes to ITNs and to quantify impact of exposure not only on instantaneous mortality, but also on blood-feeding and longevity, two traits that are central to transmission. The assays evaluated the performance of a standard ITN (Permanet® 2.0; Vestergaard Frandsen), a ‘next generation’ combination ITN with a resistance-breaking synergist (Permanet® 3.0) and an untreated net (UTN), against field-derived Anopheles gambiae sensu lato mosquitoes from Côte d’Ivoire exhibiting a 1500-fold increase in pyrethroid resistance relative to a standard susceptible strain. RESULTS: The study revealed that the standard ITN induced negligible instantaneous mortality against the resistant mosquitoes, whereas the resistance-breaking net caused high mortality and a reduction in blood-feeding. However, both ITNs still impacted long-term survival relative to the UTN. The impact on longevity depended on feeding status, with blood-fed mosquitoes living longer than unfed mosquitoes following ITN exposure. Exposure to both ITNs also reduced the blood-feeding success, the time spent on the net and blood-feeding duration, relative to the untreated net. CONCLUSION: Although a standard ITN did not have as substantial instantaneous impact as the resistance-breaking net, it still had significant impacts on traits important for transmission. These results highlight the benefit of improved bioefficacy assays that allow for realistic exposure and consider sub- or pre-lethal effects to help assess the functional significance of insecticide resistance.
Keywords	Anopheles gambiae ; hematophagy ; insecticide application ; insecticide resistance ; longevity ; malaria ; monitoring ; mortality ; pyrethrins ; Cote d'Ivoire
Language	English
Dates of publication	2022-12
Size	p. 111.
Publishing place	BioMed Central
Document type	Article
ZDB-ID	2409480-8
ISSN	1756-3305
ISSN	1756-3305
DOI	10.1186/s13071-022-05220-y
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Article: Consequences of larval competition and exposure to permethrin for the development of the rodent malaria Plasmodium berghei in the mosquito Anopheles gambiae

Hauser, Gaël / Thiévent, Kevin / Koella, Jacob C

Parasites & vectors. 2020 Dec., v. 13, no. 1

2020

Abstract: BACKGROUND: Mosquitoes and other vectors are often exposed to sublethal doses of insecticides. Larvae can be exposed to the run-off of agricultural use, and adults can be irritated by insecticides used against them and move away before they have picked ... ...

Abstract	BACKGROUND: Mosquitoes and other vectors are often exposed to sublethal doses of insecticides. Larvae can be exposed to the run-off of agricultural use, and adults can be irritated by insecticides used against them and move away before they have picked up a lethal dose. This sublethal exposure may affect the success of control of insect-borne diseases, for it may affect the competence of insects to transmit parasites, in particular if the insects are undernourished. METHODS: We assessed how exposure of larvae and adults to a sublethal dose of permethrin (a pyrethroid) and how larval competition for food affect several aspects of the vector competence of the mosquito Anopheles gambiae for the malaria parasite Plasmodium berghei. We infected mosquitoes with P. berghei and measured the longevity and the prevalence and intensity of infection to test for an effect of our treatments. RESULTS: Our general result was that the exposure to the insecticide helped mosquitoes deal with infection by malaria. Exposure of either larvae or adults decreased the likelihood that mosquitoes were infected by about 20%, but did not effect the parasite load. Exposure also increased the lifespan of infected mosquitoes, but only if they had been reared in competition. Larval competition had no effect on the prevalence of infection, but increased parasite load. These effects may be a consequence of the machinery governing oxidative stress, which underlies the responses of mosquitoes to insecticides, to food stress and to parasites. CONCLUSIONS: We conclude that insecticide residues are likely to affect the ability of mosquitoes to carry and transmit pathogens such as malaria, irrespective of the stage at which they are exposed to the insecticide. Our results stress the need for further studies to consider sublethal doses in the context of vector ecology and vector-borne disease epidemiology.
Keywords	Anopheles gambiae ; Plasmodium berghei ; larvae ; lethal dose ; longevity ; malaria ; oxidative stress ; parasite load ; parasites ; permethrin ; pyrethrins ; rodents ; runoff ; vector competence
Language	English
Dates of publication	2020-12
Size	p. 107.
Publishing place	BioMed Central
Document type	Article
Note	NAL-light
ZDB-ID	2409480-8
ISSN	1756-3305
ISSN	1756-3305
DOI	10.1186/s13071-020-3983-9
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