Biology subjects

Thomas, M. B.

Publications and source records attributed to Thomas, M. B..

9 recordsLinked to original sources

bioRxiv2025

Local adaptation of the mosquito vector, Aedes aegypti, and implications for predicting the effects of temperature and climate change on dengue transmission.

There is concern that increases in temperature due to climate change could lead to shifts in the dynamics and distribution of mosquito vectors. Many current models assume there are average thermal performance curves for a given vector species transmission. However, this one-size-fits-all assumption ignores the potential for local adaptation to create population-specific differences in thermal performance. In this study, we explored thermal performance of five independent field populations of Ae. aegypti from Mexico, together with a standard laboratory strain. We reared these six populations at temperatures between 13{degrees}C-37{degrees}C to generate thermal performance curves for a suite of life-history traits. Composite models integrating these traits revealed the effects of temperature on population growth rates and dengue virus transmission potential. The results provide strong evidence for the potential for local adaptation in Ae. aegypti populations, challenging applicability of one-size-fits-all thermal performance models to assess climate impact on mosquito-borne diseases.

ecology↗

bioRxiv2024

Thermal variation influences the transcriptome of the major malaria vector Anopheles stephensi.

The abundance and distribution of ectotherms is being shaped at unprecedented scales by human-induced climate change. Unraveling molecular adaptations to thermal variation is prescient. Vector-borne diseases are of particular concern and although mosquitoes are responsible for most of the 621 million cases annually, their response to temperature is not well characterized. We describe the transcriptome of the major vector for human malaria, Anopheles stephensi maintained under a diurnal temperature regime (DTR) totaling 9{degrees}C and daily means of 20{degrees}C, 24{degrees}C and 28{degrees}C respectively. Gene expression profiles were examined in the midguts and carcasses of adult mosquitoes from one to 19 days post-blood meal. Differences in temporal expression profiles at each temperature revealed a total of 3,106 and 3,590 genes in the carcasses and midguts respectively and analyzed further to make three inferences. First, we identified genes with shared temporal expression profiles across all three temperatures, suggesting their indispensability to mosquito life history. Second, tolerance to 20 DTR 9{degrees}C and 28 DTR 9{degrees}C was associated with a larger and more diverse repertoire of gene products compared to 24 DTR 9{degrees}C; assuming physiological costs scale accordingly, this finding could explain the fitness trade-offs underlying the unimodal effect of temperature. Third, the long duration of our study revealed two general trends in gene expression, representative of a coordinated, tissue- and temperature-specific response to blood meal digestion, managing oxidative stress, and reproduction. Our results suggest how temperature could regulate the mosquitos capacity to transmit Plasmodium parasites and offer a reference point for understanding ectotherm adaptation.

molecular biology↗

bioRxiv2023

Temperature and transmission: novel estimates of the effects of temperature on the human malaria parasite, Plasmodium falciparum

Malaria transmission is strongly influenced by traits such as mosquito life expectancy, vector competence, and the Extrinsic Incubation Period (EIP, which is the development time of the parasite inside the mosquito). Even though these traits are known to be shaped by environmental temperature and there is considerable concern that climate change could increase disease risk in certain areas, surprisingly, these temperature dependencies are poorly characterized. Here, we use a mechanistic model fitted to novel experimental data to describe how Plasmodium falciparum infection of the African malaria vector, Anopheles gambiae, is modulated by temperature, including its influences on parasite establishment, conversion efficiency through parasite developmental stages, EIP and overall competence. We use these data, together with novel estimates of the survival of infected blood-fed mosquitoes, to explore the potential influence of temperature on transmission in four locations in Kenya, considering recent conditions and future climate change. Results provide insights into factors limiting transmission in cooler environments and indicate that increases in malaria transmission efficiency due to climate warming in areas like the Kenyan Highlands, might be less than previously predicted.

microbiology↗

bioRxiv2021

Omitting age-dependent mosquito mortality in malaria models underestimates the effectiveness of insecticide-treated nets

Mathematical models of vector-borne infections, including malaria, often assume age-independent mortality rates of vectors, despite evidence that many insects senesce. In this study we present survival data on insecticide-resistant Anopheles gambiae s.l. from experiments in Cote dIvoire. We fit a constant mortality function and two age-dependent functions (logistic and Gompertz) to the data from mosquitoes exposed (treated) and not exposed (control) to insecticide-treated nets (ITNs), to establish biologically realistic survival functions. This enables us to explore the effects of insecticide exposure on mosquito mortality rates, and the extent to which insecticide resistance might impact the effectiveness of ITNs. We investigate this by calculating the expected number of infectious bites a mosquito will take in its lifetime, and by extension the vectorial capacity. Our results show that the predicted vectorial capacity is substantially lower in mosquitoes exposed to ITNs, despite the mosquitoes in the experiment being highly insecticide-resistant. The more realistic age-dependent functions provide a better fit to the experimental data compared to a constant mortality function and, hence, influence the predicted impact of ITNs on malaria transmission potential. In models with age-independent mortality, there is a great reduction for the vectorial capacity under exposure compared to no exposure. However, the two age-dependent functions predicted an even larger reduction due to exposure, highlighting the impact of incorporating age in the mortality rates. These results further show that multiple exposures to ITNs had a considerable effect on the vectorial capacity. Overall, the study highlights the importance of including age dependency in mathematical models of vector-borne disease transmission and in fully understanding the impact of interventions. Author summaryInterventions against malaria are most commonly targeted on the adult mosquitoes, which transmit the infection from person to person. One of the most important interventions are bed-nets, treated with insecticides. Unfortunately, extensive exposure of mosquitoes to insecticide has led to widespread evolution of insecticide resistance, which might threaten control strategies. Piecing together the overall impact of resistance on the efficacy of insecticide-treated nets is complex, but can be informed by the use of mathematical models. However, there are some assumptions that the models frequently use which are not realistic in terms of the mosquito biology. In this paper, we formulate a model that includes age-dependent mortality rates, an important parameter in vector control since control strategies most commonly aim to reduce the lifespan of the mosquitoes. By using novel data collected using field-derived insecticide-resistant mosquitoes, we explore the effects that the presence of insecticides on nets have on the mortality rates, as well as the difference incorporating age dependency in the model has on the results. We find that including age-dependent mortality greatly alters the anticipated effects of insecticide-treated nets on mosquito transmission potential, and that ignoring this realism potentially overestimates the negative impact of insecticide resistance.

ecology↗

bioRxiv2020

Using a non-destructive sugar-feeding assay for sporozoite detection and estimating the extrinsic incubation period of Plasmodium falciparum in mosquito vectors

Despite its epidemiological importance, the time Plasmodium parasites take to achieve development in the vector mosquito (the extrinsic incubation period, EIP) remains poorly characterized. A novel non-destructive assay designed to estimate EIP in single mosquitoes, and more broadly to study Plasmodium - Anopheles vectors interactions, is presented. The assay uses small pieces of cotton wool soaked in sugar solution to collect malaria sporozoites from individual mosquitoes during sugar feeding to monitor infection status over time. This technique has been tested across four natural malaria mosquito species of Africa and Asia, six parasite isolates of Plasmodium falciparum, and across a range of temperatures relevant to malaria transmission in field conditions. We find that monitoring individual infectious mosquitoes is feasible, although due to the frequency of mosquito sugar feeding and inter-individual variation in infection intensity, there is inherent risk that this technique will result in some false negatives. The sensitivity rate ranged from 0.27 to 0.81 depending on mosquito species and on infection intensity in mosquitoes used to collect saliva. Using this non-destructive technique, the estimated median extrinsic incubation period of P. falciparum at 27{degrees}C was 11 to 14 days depending on mosquito species and parasite isolate. Long-term individual tracking also revealed that sporozoite transfer onto cotton wool can occur at least until day 40 post-infection. In addition to contributing to a better understanding of EIP and mosquito to human transmission with implications for improving epidemiological models, this technique also allows to link different transmission traits at the mosquito individual level. As one example, we found a significant relationship between EIP and mosquito lifespan, with short individual EIP associated with short mosquito lifespan. Correlations between mosquito/parasite traits often reveal trade-offs and constraints and have important implications for understanding the evolution of parasite transmission strategies.

molecular biology↗

bioRxiv2019

Field relevant variation in ambient temperature modifies the density-dependent establishment of Plasmodium falciparum in mosquitoes: implications for the infectious reservoir and beyond?

The relationship between Plasmodium falciparum gametocyte density and infections in mosquitoes is central to understanding the rates of transmission with important implications for control. Here, we determined whether field relevant variation in environmental temperature could also modulate this relationship. Anopheles stephensi were challenged with three densities of P. falciparum gametocytes spanning a [~]10-fold gradient, and housed under diurnal/daily temperature range (\"DTR\") of 9{degrees}C around means of 20{degrees}C, 24{degrees}C and 28{degrees}C. At the peak stages of infection for each temperature, the proportion of mosquitoes infected with oocysts in the midguts or infectious with sporozoites in the salivary glands were measured (referred to collectively as vector competence hereon), in addition to oocyst intensities from infected midguts. While vector competence was similar at 20 DTR 9{degrees}C and 24 DTR 9{degrees}C, the proportion of mosquitoes infected and subsequently infectious were also comparable, with evidence, surprisingly, for higher vector competence in mosquitoes challenged with intermediate gametocyte densities. For the same gametocyte densities however, severe reduction in the proportion of infectious mosquitoes was accompanied by a significant decline in vector competence at 28 DTR 9{degrees}C, although density per se showed a positive and linear effect at this temperature. Unlike vector competence, oocyst intensities decreased with increasing temperatures with a predominantly positive and linear association with gametocyte density, especially at 28 DTR 9{degrees}C. Oocyst intensities across individual infected midguts suggested temperature-specific differences in mosquito susceptibility/resistance: at 20 DTR 9{degrees}C and 24 DTR 9{degrees}C, dispersion (aggregation) increased in a density-dependent manner but not at 28 DTR 9{degrees}C where the distributions were consistently random. Limitations notwithstanding, our results have manifold implications in, for instance, how variation in temperature could modify seasonal dynamics of infectious reservoirs and transmission and the contribution of high-/patent- and low-density/sub-patent carriers, to suggestions for design and deployment of transmission-blocking vaccines/drugs, but with a cautionary note suggesting how low efficacy could lead to transmission enhancement in certain environments.

ecology↗

bioRxiv2019

Thermal ecology of malaria transmission and the potential impact of behavioural resistance

Insecticide-treated bed nets reduce malaria transmission by limiting contact between mosquito vectors and human hosts when mosquitoes feed during the night. However, malaria vectors can also feed in the early evening and in the morning when people are not protected. Here, we explored how timing of blood feeding interacts with environmental temperature to influence the capacity of Anopheles mosquitoes to transmit the human malaria parasite, Plasmodium falciparum. We found no effect of biting time itself on the proportion of mosquitoes that became infectious (vector competence) at constant temperature. However, when mosquitoes were maintained under more realistic fluctuating temperatures there was a significant increase in competence for mosquitoes feeding in the evening, and a significant reduction in competence for those feeding in the morning, relative to those feeding at midnight. These effects appear to be due to thermal sensitivity of malaria parasites during the initial stages of parasite development within the mosquito, and the fact that mosquitoes feeding in the evening experience cooling temperatures during the night, whereas mosquitoes feeding in the morning quickly experience warming temperatures that are inhibitory to parasite establishment. A transmission dynamics model illustrates that such differences in competence could have important implications for disease endemicity, the extent of transmission that persists in the presence of bed nets, and the epidemiological impact of behavioural resistance. These results indicate the interaction of temperature and feeding behaviour to be a major ecological determinant of the vectorial capacity of malaria mosquitoes.

ecology↗

bioRxiv2019

Exploring the lower thermal limits for transmission of human malaria, Plasmodium falciparum

The rate of malaria transmission is strongly determined by parasite development time in the mosquito, known as the extrinsic incubation period (EIP), since the quicker parasites develop, the greater the chance that the vector will survive long enough for the parasite to complete development and be transmitted. EIP is known to be temperature dependent but this relationship is surprisingly poorly characterized. There is a single degree-day model for EIP of Plasmodium falciparum that derives from a limited number of poorly controlled studies conducted almost a century ago. Here, we show that the established degree-day model greatly underestimates the rate of development of P. falciparum in both Anopheles stephensi and An. gambiae mosquitoes at temperatures in the range of 17-20{degrees}C. We also show that realistic daily temperature fluctuation further speeds parasite development. These novel results challenge one of the longest standing models in malaria biology and have potentially important implications for understanding the impacts of climate change.

ecology↗

bioRxiv2018

More than a flying syringe: Using functional traits in vector borne disease research

Many important endemic and emerging diseases are vector-borne. The functional traits of vectors affect not just pathogen transmission rates, but also the fitness and population dynamics of these animals themselves. Increasing empirical evidence suggests that vector traits vary significantly at time scales relevant to transmission dynamics. Currently, an understanding of how this variation in key traits impacts transmission is hindered by a lack of both empirical data and theoretical methods for mechanistically incorporating traits into transmission models. Here, we present a framework for incorporating both intrinsic and environment-driven variation in vector traits into empirical and theoretical vector-borne disease research. This framework mechanistically captures the effect of trait variation on vector fitness, the correlation between vector traits, and how these together determine transmission dynamics. We illustrate how trait-based vector-borne disease modelling can make novel predictions, and identify key steps and challenges in the construction, empirical parameterisation and validation of such models, as well as the organization and prioritization of data collection efforts.

ecology↗