Ecological Immunology of mosquito-malaria interactions: Of non-natural versus natural model systems and their inferences

Abstract

There has been a recent shift in the literature on mosquito/Plasmodium interactions with an increasingly large number of theoretical and experimental studies focusing on their population biology and evolutionary processes. Ecological immunology of mosquito-malaria interactions -the study of the mechanisms and function of mosquito immune responses to Plasmodium in their ecological and evolutionary context -is particularly important for our understanding of malaria transmission and how to control it. Indeed, describing the processes that create and maintain variation in mosquito immune responses and parasite virulence in natural populations may be as important to this endeavor as describing the immune responses themselves. For historical reasons, Ecological Immunology still largely relies on studies based on non-natural model systems. There are many reasons why current research should favour studies conducted closer to the field and more realistic experimental systems whenever possible. As a result, a number of researchers have raised concerns over the use of artificial host-parasite associations to generate inferences about population-level processes. Here I discuss and review several lines of evidence that, I believe, best illustrate and summarize the limitations of inferences generated using nonnatural model systems.Key words: Anopheles gambiae, Plasmodium falciparum, mosquito-malaria interactions, model systems, inferences, ecological immunology, micro-coevolution, macro-coevolution life history trade-offs, transcriptomes. I N T R O D U C T I O NThe majority of malaria-associated human mortality is caused by Plasmodium falciparum, a haemosporidian parasite of man that occurs in most tropical and sub-tropical regions of the world and is transmitted by anopheline mosquito species. It has long been recognized that understanding the mosquito immune response to infection by P. falciparum may be the key to finding ways of interrupting its transmission. Thus parasitologists and, more recently, insect molecular biologists have focused their research on mosquito immune-related genes and particularly on genes responsible for mosquito refractoriness to the malaria parasite, as well as on parasite-induced fitness costs to mosquito vectors. Since experimental infections of humans or primates are usually not possible much of that research is based on vertebrate/ mosquito/Plasmodium model-systems which, as will be discussed in the next sections, often involve mosquito/Plasmodium associations that do not occur in nature.Ecological immunology is a relatively new discipline that focuses on the mechanism and function of immune responses in their ecological context. Since its focus is on population level processes, ecological immunology uses naturally-occurring host-parasite association as model systems. When it comes to research on mosquito/Plasmodium interactions, ecological immunology investigates how ecological factors affect interactions between mosquito vectors and the malaria parasite to create and maintain variation in ho...

Plasmodium falciparum Produce Lower Infection Intensities in Local versus Foreign Anopheles gambiae Populations

“…The likely dynamic nature of vector-parasite interactions could mean that much of the current research that does not take this into account may have been misinterpreted [25]. This study reiterates what has previously been suggested that researching vector-parasite interactions in unnatural couples, which could be due to using lab strains, artificial species combinations or simply geographically isolated vectors and parasites, molecular interactions uncovered could differ drastically to those found in nature [7], [63]–[64]. On top of that, on uncovering a molecular basis to, for example, mosquito resistance to malaria, the magnitude of its effect cannot be determined until it is tested in multiple sympatric couples.…”

“…Selective pressures exerted by the parasite on its host and vice versa are expected to drive evolution for each to maximize its fitness. In the vectorial stages, evolutionary forces will favor the parasites with the highest transmission [7], this could lead to adaptation between sympatric parasite and vector populations due to local adaptation [8]. The factors that regulate the success and level of infection in the malaria vectors are now under scrutiny but the role of natural population diversity and geographical variations remain overlooked.…”

Exposure of the mosquito vector Culex pipiens to the malaria parasite Plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival

“…Furthermore, the isolation of individuals from the wild to controlled laboratory conditions for several generations alters the selective pressures imposed on them and may modify the expression of wild traits. In research conducted on vector- Plasmodium , studies may differ substantially in terms of these characteristics [62]. Here, we studied a natural ( Culex pipiens - Plasmodium relictum ) and wild (mosquitoes hatched from clutches collected on the field and Plasmodium strain was isolated since two years) vector-parasite association.…”

Insecticide resistance and malaria transmission: infection rate and oocyst burden in Culex pipiens mosquitoes infected with Plasmodium relictum

“…This may increase the chances of detecting an eventual pleiotropic effect of the insecticide resistance genes, but the results may not be necessarily applicable to other genetic backgrounds, particularly if there are epistatic interactions between the insecticide resistant genes and other genes in the genome (although modifier genes have not yet been described in this species [33]). The field-collected mosquitoes, on the other hand, allowed us to test the effects under the more realistic conditions of a heterogeneous genetic background [34]. Combined, these two approaches provide a powerful test of the role of insecticide resistance on parasite development within the mosquito.…”