Project

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Resource ecology of host-parasite interactions and evolution

Applicant Koella Jacob
Number 144207
Funding scheme Project funding (Div. I-III)
Research institution Institut de Biologie Faculté des Sciences Université de Neuchâtel
Institution of higher education University of Neuchatel - NE
Main discipline Ecology
Start/End 01.02.2013 - 30.06.2016
Approved amount 547'330.00
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Keywords (4)

resource ecology; virulence; parasite evolution; host-parasite interactions

Lay Summary (English)

Lead
Lay summary

Why do some parasites, like the common cold viruses, cause very little harm to their hosts, while others, like the plague bacterium, kill them very rapidly? There are, broadly speaking, two approaches to answer this question. On the one hand, we try to understand the mechanistic basis of the host-parasite interaction: its molecular and cellular biology and its physiology. On the other hand, we try to understand the evolutionary pressures shaping the interaction. Most of our evolutionary ideas are formulated within a framework assuming that increased virulence is the unavoidable consequence of a higher rate of the parasite’s transmission, i.e. that there is a trade-off between virulence and rate of transmission.

Each approach has developed more or less independently of the other, leaving each somewhat unsatisfactory and preventing a complete picture of host-parasite evolution.

With the work of this proposal, I will try to give a mechanistic basis to the evolutionary ideas underlying host-parasite interactions by considering them in the context of resource ecology. This takes into account a fundamental aspect of parasites that, however, is generally ignored: that they steal resources from their host to support their own development. The approach asks how the availability of the host’s resources constrains its own and its parasite’s growth, and how their evolutionary strategies of both change according to both partner’s resource-based constraints.

The project deals with the microsporidian Vavraia culicis and its host, the mosquito Aedes aegypti. Developing mathematical theory in close contact with experimental studies that test the model’s assumptions and predictions, I will approach the problem in three steps.

First, I will adapt models of individual development to show how the availability of resources (and thus energy) constrains the mosquito’s growth. This environmental constraint, in turn, will influence the developmental strategy used by the mosquito to achieve its reproductive success. Explaining variation of such strategies is the aim of life-history theory. This first step is thus essentially an attempt to introduce mechanistic descriptions of individual growth into life-history theory.

Second, as the parasite’s growth depends on the resources it obtains from its host, it will affect the host’s energy budget; the model of individual growth will be modified accordingly.  This will enable me to answer two sets of questions. (i) How do the host’s resources affect the parasite’s growth and epidemiological parameters associated with parasite load: its transmission rate and virulence? (ii) How does the parasite affect the host’s growth and thus its optimal life-history?

Third, while the parasite’s virulence and transmission are constrained by the growth within its host, its evolution is determined by its epidemiological dynamics. I will therefore combine the models linking resource ecology to within-host dynamics of the parasite with models describing its epidemiology. This gives the possibility to reach the goal of the project: to describe the evolution of the parasite’s virulence as a function of its host’s resources.

Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
A genetic model of the effects of insecticide-treated bed nets on the evolution of insecticide-resistance
Birget PLG, Koella JC (2016), A genetic model of the effects of insecticide-treated bed nets on the evolution of insecticide-resistance, in Evolution in Medicine and Public Health, @015, 205.
Effects of food variability on growth and reproduction of Aedes aegypti.
Zeller M, koella JC (2016), Effects of food variability on growth and reproduction of Aedes aegypti., in Ecology and Evolution , 6, 552.
Overloading the immunity of the mosquito Anopheles gambiae with multiple immune challenges
Barreaux AP, Barreaux P, Koella JC (2016), Overloading the immunity of the mosquito Anopheles gambiae with multiple immune challenges, in Parasites & Vectors, 9, 210.
An epidemiological model of the effects of insecticide-treated bed nets on malaria transmission
Birget PLG, Koella JC (2015), An epidemiological model of the effects of insecticide-treated bed nets on malaria transmission, in PLoS ONE, 10, e0144173.
Larval and adult environmental temperatures influence the adult reproductive traits of Anopheles gambiae s.s
Christiansen-Jucht C, Parham PE, Saddler A, Koella JC, Basáñez M-G (2015), Larval and adult environmental temperatures influence the adult reproductive traits of Anopheles gambiae s.s, in Parasites & Vectors , 8, 456.
Modelling the impact of declining insecticide resistance with mosquito age on malaria
Saddler A, Koella JC (2015), Modelling the impact of declining insecticide resistance with mosquito age on malaria, in Malaria World Journal , 6, 13.
Resisting infection by Plasmodium berghei increases the sensitivity of the malaria vector Anopheles gambiae to DDT
Saddler A, Burda P-C, Koella JC (2015), Resisting infection by Plasmodium berghei increases the sensitivity of the malaria vector Anopheles gambiae to DDT, in Malaria Journal, 14, 134.
Temperature during larval development and adult maintenance influences the survival of Anopheles gambiae ss
Christiansen-Jucht C, Parham PE, Saddler A, Koella JC, Basanez M-G (2014), Temperature during larval development and adult maintenance influences the survival of Anopheles gambiae ss, in Parasites and vectors, 7, 489.
Effects of age and larval nutrition on phenotypic expression of insecticide-resistance in Anopheles mosquitoes
Kulma K, Saddler A, Koella JC (2013), Effects of age and larval nutrition on phenotypic expression of insecticide-resistance in Anopheles mosquitoes, in PLoS ONE, 8, e58322.
Plasmodium-Anopheles interactions: understanding what’s best for the parasite and mosquito
Slater HC, Churcher TS, Christophides GK, Koella JC, Basanez M-G (2013), Plasmodium-Anopheles interactions: understanding what’s best for the parasite and mosquito, in Pathogens and Global Health , 107, 404.
The influence of Dengue virus serotype-2 infection on Aedes aegypti (Diptera: Culicidae) motivation and avidity to blood feed
Maciel de Freitas R, Sylvestre RG, Gandini M, koella JC (2013), The influence of Dengue virus serotype-2 infection on Aedes aegypti (Diptera: Culicidae) motivation and avidity to blood feed, in PLoS ONE, 8, e65252.

Associated projects

Number Title Start Funding scheme
192786 Resource ecology of the growth and virulence of parasites 01.05.2020 Project funding (Div. I-III)
192786 Resource ecology of the growth and virulence of parasites 01.05.2020 Project funding (Div. I-III)
169842 Integrating resistance and tolerance to parasitic infection with life-history theory 01.11.2016 Project funding (Div. I-III)

Abstract

Ideas about the evolution of host-parasite systems have been developed for decades, but their empirical validation remains problematic. One reason is that most theoretical models are based on assumptions that are difficult to test in biological systems. A common assumption is, for example, that increased virulence is the unavoidable consequence of a higher rate of the parasite’s transmission, i.e. that there is a trade-off between virulence and rate of transmission. This trade-off hypothesis has given a simple framework, within which new ideas can be formulated and tested at least qualitatively. Nevertheless, the hypothesis remains unsatisfying, for although changes in the shape of the trade-off - whether it is convex, linear or concave - can radically affect the outcome of evolution, it is difficult to identify the shape and thus to make quantitative predictions about particular host-parasite systems. A helpful step forward has been to consider the trade-off as a naturally emerging consequence of the dynamics of the parasite within its host, but we now need better knowledge - both theoretical and empirical - of these within-host dynamics and of the resulting host-parasite interactions. I suggest that one way to help reach this goal (out of several possible ones, including, e.g., modern developments in immuno-pathology) is to consider parasite-host evolution in the context of resource ecology. This explicitly takes into account a fundamental aspect of parasites that is generally ignored: that they steal resources from their host to support their own development. Resource ecology thus gives a mechanistic basis of the host’s and the parasite’s development, and thereby brings theory in closer contact with experimental observations, leading to a more realistic description of the host-parasite interaction. This project deals with the microsporidian Vavraia culicis and its host, the mosquito Aedes aegypti. Starting with a resource-based model of ontogenetic growth, it combines theory and experiments to study the mechanistic basis and the evolution of the interaction between the host and the parasite. It has three aims.1. Predict the host’s optimal life-history, using a resource-based model of the mosquito’s ontogenetic growth. We will adapt a model of ontogenetic growth, which is based on the balance of energy during the host’s development, to describe how variation in resource availability affects the mosquito’s growth; we will measure the metabolic parameters of the model, use the model to predict the mosquito’s evolutionarily optimal life-history, and test the predictions with an experimental evolution approach that compares the evolutionary outcome of different larval diets.2. Describe the within-host dynamics and host-parasite interactions. We will extend the model of ontogenetic growth by including the within-host dynamics of the parasite to explore how resource availability constrains the parasite’s development, to describe the influence of the parasite on the evolutionary pressures on the host’s life-history, and to predict the outcome of infection with regard to two important epidemiological parameters: virulence and transmission. Lab experiments will answer questions about the model’s assumptions, such as: What proportion of the host’s resources is used by the parasite? Does the host’s body size lead to density-dependence of the parasite’s growth and pathogenic effects? How does parasite load relate to the probability of the host’s death? Other experiments will test predictions about the shape of epidemiologically relevant trade-offs as a function of resource availability.3. Predict the effect of host resources on the evolution of the parasite. We will combine the model of within-host dynamics described above with an epidemiological model of the parasite’s dynamics among hosts to predict the evolutionary dynamics of the parasite as a function of the host’s resources. We will then test the predictions with an experimental evolution approach that compares how the parasite’s development evolves in response to the host’s larval diet.
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