Alterations in Mosquito Behaviour by Malaria Parasites: Potential Impact on Force of Infection

A variety of studies have reported that malaria parasites alter the behaviour of mosquitoes. These behavioural alterations likely increase transmission because they reduce the risk of vector death during parasite development and increase biting after parasites become infectious. A mathematical model is used to investigate the potential impact of these behavioural alterations on the lifetime number of infectious bites delivered. The model is used to explore the importance of assumptions about the magnitude and distribution of mortality as well as the importance of extrinsic incubation period and gonotrophic cycle length. Additionally, the model is applied to four datasets taken from actual transmission settings. The impact of behavioural changes on the relative number of lifetime bites is highly dependent on assumptions about the distribution of mortality over the mosquito-feeding cycle. Even using fairly conservative estimates of these parameters and field collected data, the model outputs suggest that altered feeding could easily cause a doubling in the force of infection.Infection-iduced behavioural alterations have their greatest impact on the lifetime number of infectious bites in environments with high feeding-related adult mortality and many pre-infectious feeding cycles. Interventions that increase feeding-associated mortality are predicted to amplify the relative fitness benefits and hence enhance the strength of selection for behavioural alteration\u

Competition and resource depletion shape the thermal response of population fitness in Aedes aegypti.

Mathematical models that incorporate the temperature dependence of lab-measured life history traits are increasingly being used to predict how climatic warming will affect ectotherms, including disease vectors and other arthropods. These temperature-trait relationships are typically measured under laboratory conditions that ignore how conspecific competition in depleting resource environments-a commonly occurring scenario in nature-regulates natural populations. Here, we used laboratory experiments on the mosquito Aedes aegypti, combined with a stage-structured population model, to investigate this issue. We find that intensified larval competition in ecologically-realistic depleting resource environments can significantly diminish the vector's maximal population-level fitness across the entire temperature range, cause a ~6 °C decrease in the optimal temperature for fitness, and contract its thermal niche width by ~10 °C. Our results provide evidence for the importance of considering intra-specific competition under depleting resources when predicting how arthropod populations will respond to climatic warming

Fitness consequences of altered feeding behavior in immune-challenged mosquitoes

Background: Malaria-infected mosquitoes have been reported to be more likely to take a blood meal when parasites are infectious than when non-infectious. This change in feeding behavior increases the likelihood of malaria transmission, and has been considered an example of parasite manipulation of host behavior. However, immune challenge with heat-killed Escherichia coli induces the same behavior, suggesting that altered feeding behavior may be driven by adaptive responses of hosts to cope with an immune response, rather than by parasite-specific factors. Here we tested the alternative hypothesis that down-regulated feeding behavior prior to infectiousness is a mosquito adaptation that increases fitness during infection. Methods: We measured the impact of immune challenge and blood feeding on the fitness of individual mosquitoes. After an initial blood meal, Anopheles stephensi Liston mosquitoes were experimentally challenged with heat-killed E. coli at a dose known to mimic the same temporal changes in mosquito feeding behavior as active malaria infection. We then tracked daily egg production and survivorship of females maintained on blood-feeding regimes that either mimicked down-regulated feeding behaviors observed during early malaria infection, or were fed on a four-day feeding cycle typically associated with uninfected mosquitoes. Results: Restricting access to blood meals enhanced mosquito survival but lowered lifetime reproduction. Immune-challenge did not impact either fitness component. Combining fecundity and survival to estimate the population-scale intrinsic rate of increase (r), we found that, contrary to the mosquito adaptation hypothesis, mosquito fitness decreased if blood feeding was delayed following an immune challenge. Conclusions: Our data provide no support for the idea that malaria-induced suppression of blood feeding is an adaptation by mosquitoes to reduce the impact of immune challenge. Alternatively, the behavioral alterations may be neither host nor parasite adaptations, but rather a consequence of constraints imposed on feeding by activation of the mosquito immune response, i.e. non-adaptive illness-induced anorexia. Future work incorporating field conditions and different immune challenges could further clarify the effect of altered feeding on mosquito and parasite fitness

The Role of Vector Trait Variation in Vector-Borne Disease Dynamics

Many important endemic and emerging diseases are transmitted by vectors that are biting arthropods. The functional traits of vectors can affect pathogen transmission rates directly and also through their effect on vector population dynamics. Increasing empirical evidence shows that vector traits vary significantly across individuals, populations, and environmental conditions, and at time scales relevant to disease transmission dynamics. Here, we review empirical evidence for variation in vector traits and how this trait variation is currently incorporated into mathematical models of vector-borne disease transmission. We argue that mechanistically incorporating trait variation into these models, by explicitly capturing its effects on vector fitness and abundance, can improve the reliability of their predictions in a changing world. We provide a conceptual framework for incorporating trait variation into vector-borne disease transmission models, and highlight key empirical and theoretical challenges. This framework provides a means to conceptualize how traits can be incorporated in vector borne disease systems, and identifies key areas in which trait variation can be explored. Determining when and to what extent it is important to incorporate trait variation into vector borne disease models remains an important, outstanding question

Variable responses of individual species to tropical forest degradation

The functional stability of ecosystems depends greatly on interspecific differences in responses to environmental perturbation. However, responses to perturbation are not necessarily invariant among populations of the same species, so intraspecific variation in responses might also contribute. Such inter-population response diversity has recently been shown to occur spatially across species ranges, but we lack estimates of the extent to which individual populations across an entire community might have perturbation responses that vary through time. We assess this using 524 taxa that have been repeatedly surveyed for the effects of tropical forest logging at a focal landscape in Sabah, Malaysia. Just 39 % of taxa – all with non-significant responses to forest degradation – had invariant responses. All other taxa (61 %) showed significantly different responses to the same forest degradation gradient across surveys, with 6 % of taxa responding to forest degradation in opposite directions across multiple surveys. Individual surveys had low power (< 80 %) to determine the correct direction of response to forest degradation for one-fifth of all taxa. Recurrent rounds of logging disturbance increased the prevalence of intra-population response diversity, while uncontrollable environmental variation and/or turnover of intraspecific phenotypes generated variable responses in at least 44 % of taxa. Our results show that the responses of individual species to local environmental perturbations are remarkably flexible, likely providing an unrealised boost to the stability of disturbed habitats such as logged tropical forests

Thresholds for adding degraded tropical forest to the conservation estate

Logged and disturbed forests are often viewed as degraded and depauperate environments compared with primary forest. However, they are dynamic ecosystems1 that provide refugia for large amounts of biodiversity2,3, so we cannot afford to underestimate their conservation value4. Here we present empirically defined thresholds for categorizing the conservation value of logged forests, using one of the most comprehensive assessments of taxon responses to habitat degradation in any tropical forest environment. We analysed the impact of logging intensity on the individual occurrence patterns of 1,681 taxa belonging to 86 taxonomic orders and 126 functional groups in Sabah, Malaysia. Our results demonstrate the existence of two conservation-relevant thresholds. First, lightly logged forests (68%) of their biomass removed, and these are likely to require more expensive measures to recover their biodiversity value. Overall, our data confirm that primary forests are irreplaceable5, but they also reinforce the message that logged forests retain considerable conservation value that should not be overlooked

Data from: Size, sounds and sex: interactions between body size and harmonic convergence signals determine mating success in Aedes aegypti

Background: Several new mosquito control strategies will involve the release of laboratory reared males which will be required to compete with wild males for mates. Currently, the determinants of male mating success remain unclear. The presence of convergence between male and female harmonic flight tone frequencies during a mating attempt have been found to increase male mating success in the yellow fever mosquito, Aedes aegypti. Size has also been implicated as a factor in male mating success. Here, we investigated the relationships among body size, harmonic convergence signalling, and mating success. We predicted that harmonic convergence would be an important determinant of mating success and that large individuals would be more likely to converge. Methods: We used diet to manipulate male and female body size and then measured acoustic interactions during mating attempts between pairs of different body sizes. Additionally, we used playback experiments to measure the direct effect of size on signalling performance. Results: In live pair interactions, harmonic convergence was found to be a significant predictor of copula formation. However, we also found interactions between harmonic convergence behaviour and body size. The probability that a given male successfully formed a copula was a consequence of his size, the size of the female encountered, and whether or not they converged. While convergence appears to be predictive of mating success regardless of size, the positive effect of convergence was modulated by size combinations. In playbacks, adult body size did not affect the probability of harmonic convergence responses. Conclusions: Both body size and harmonic convergence signalling were found to be determinants of male mating success. Our results suggest that in addition to measuring convergence ability of mass release lines that the size distribution of released males may need to be adjusted to complement the size distribution of females. We also found that diet amount alone cannot be used to increase male mating success or convergence probability. A clearer understanding of convergence behaviours, their relationship to mating success, and factors influencing convergence ability would provide the groundwork for improving the mating performance of laboratory reared lines

Live Recording Playback Summary

Summary information for each test mosquito provided live recording playbacks

Live Recording Playback Detailed

Data on acoustic response for each live recording playback pulse for each test mosquito. Each mosquito has unique ID number