Christine Chevillon

Insecticide resistance genes induce a mating competition cost in Culex pipiens mosquitoes

Resistance to organophosphorus insecticides (OP) in Culex pipiens mosquitoes represents a convenient model for investigating the fitness cost of resistance genes and its origin, since both the environmental changes in nature and the adaptive genes are clearly identified. Two loci are involved in this resistance--the super-locus Ester and the locus Ace.1--each displaying several resistance alleles. Population surveys have shown differences in fitness cost between these resistance genes and even between resistance alleles of the same locus. In order to better understand this fitness cost and its variability, the effects of these resistance genes on several fitness-related traits are being studied. Here, through competition experiments between two males for the access to one female, we analysed the effect on paternity success associated with three resistance alleles--Ester4, Ester1 and Ace.1R--relative to susceptible males and relative to one another. The eventual effect of female genotype on male mating success was also studied by using susceptible and resistant females. The strains used in this experiment had the same genetic background. Susceptible males had a mating advantage when competing with any of the resistant males, suggesting a substantial cost of resistance genes to this trait. When competing against susceptible males, the paternity success did not vary among resistant males, whatever the genotype of the female. When competing against other resistant males, no difference in paternity success was apparent, except when the female was Ester1.

Insecticide resistance in the mosquito Culex pipiens: what have we learned about adaptation?

Resistance to organophosphate (OP) insecticide in the mosquito Culex pipiens has been studied for ca. 30 years. This example of micro-evolution has been thoroughly investigated as an opportunity to assess precisely both the new adapted phenotypes and the associated genetic changes. A notable feature is that OP resistance is achieved with few genes, and these genes have generally large effects. The molecular events generating such resistance genes are complex (e.g., gene amplification, gene regulation) potentially explaining their low frequency of de novo occurrence. In contrast, migration is a frequent event, including passive transportation between distant populations. This generates a complex interaction between mutations and migration, and promotes competition among resistance alleles. When the precise physiological action of each gene product is rather well known, it is possible to understand the dominance level or the type of epistasis observed. It is however difficult to predict a priori how resistance genes will interact, and it is too early to state whether or not this will be ever possible. These resistance genes are costly, and the cost is variable among them. It is usually believed that the initial fitness cost would gradually decrease due to subsequent mutations with a modifier effect. In the present example, a particular modifier occurred (a gene duplication) at one resistance locus, whereas at the other one reduction of cost is driven by allele replacement and apparently not by selection of modifiers.

FITNESS COSTS OF INSECTICIDE RESISTANCE IN NATURAL BREEDING SITES OF THE MOSQUITO CULEX PIPIENS

Abstract Genetic changes conferring adaptation to a new environment may induce a fitness cost in the previous environment. Although this prediction has been verified in laboratory conditions, few studies have tried to document this cost directly in natural populations. Here, we evaluated the pleiotropic effects of insecticide resistance on putative fitness components of the mosquito Culex pipiens. Experiments using different larval densities were performed during the summer in two natural breeding sites. Two loci that possess alleles conferring organophosphate (OP) resistance were considered: ace‐1 coding for an acetylcholinesterase (AChE1, the OP target) and Ester, a “super locus” including two closely linked loci coding for esterases A and B. Resistance ace‐1 alleles coding for a modified AChE1 were associated with a longer development time and shorter wing length. The pleiotropic effects of two resistance alleles Ester1 and Ester4 coding for the overproduced esterases A1 and A4‐B4, respectively, were more variable. Both A1 and A4‐B4 reduced wing length, although only A1 was associated with a longer preimaginal stage. The fluctuating asymmetry (FA) of the wing did not respond to the presence or to the interaction of resistance alleles at the two loci at any of the density levels tested. Conversely, the FA of one wing section decreased when larval density increased. This may be the consequence of selection against less developmentally stable individuals. The results are discussed in relation to the local evolution of insecticide resistance genes.

Genetic specificity and potential for local adaptation between dengue viruses and mosquito vectors

BackgroundSeveral observations support the hypothesis that vector-driven selection plays an important role in shaping dengue virus (DENV) genetic diversity. Clustering of DENV genetic diversity at a particular location may reflect underlying genetic structure of vector populations, which combined with specific vector genotype × virus genotype (G × G) interactions may promote adaptation of viral lineages to local mosquito vector genotypes. Although spatial structure of vector polymorphism at neutral genetic loci is well-documented, existence of G × G interactions between mosquito and virus genotypes has not been formally demonstrated in natural populations. Here we measure G × G interactions in a system representative of a natural situation in Thailand by challenging three isofemale families from field-derived Aedes aegypti with three contemporaneous low-passage isolates of DENV-1.ResultsAmong indices of vector competence examined, the proportion of mosquitoes with a midgut infection, viral RNA concentration in the body, and quantity of virus disseminated to the head/legs (but not the proportion of infected mosquitoes with a disseminated infection) strongly depended on the specific combinations of isofemale families and viral isolates, demonstrating significant G × G interactions.ConclusionEvidence for genetic specificity of interactions in our simple experimental design indicates that vector competence of Ae. aegypti for DENV is likely governed to a large extent by G × G interactions in genetically diverse, natural populations. This result challenges the general relevance of conclusions from laboratory systems that consist of a single combination of mosquito and DENV genotypes. Combined with earlier evidence for fine-scale genetic structure of natural Ae. aegypti populations, our finding indicates that the necessary conditions for local DENV adaptation to mosquito vectors are met.

The Chikungunya threat: an ecological and evolutionary perspective

Chikungunya virus (CHIKV) is an emerging mosquito-borne alphavirus. Although primarily African and zoonotic, it is known chiefly for its non-African large urban outbreaks during which it is transmitted by the same vectors as those of Dengue viruses. Unlike Dengue viruses, CHIKV displays a re-emergence pattern that closely depends on long-distance migrations including recent re-immigrations from African (putatively zoonotic) sources. Genus-based differences also emerged when comparing the evolution of Dengue-related (Flaviviruses) and of CHIKV-related (Alphaviruses) arboviruses. In this review, we discuss current information on CHIKV genetics, ecology and human infection. Further investigations on African CHIKV ecology and the differences between Flavivirus and Alphavirus members in adaptive changes and evolutionary constraints are likely to help delineate the potential of further CHIKV (re-)emergence.

EVOLUTION OF RESISTANCE IN CULEX PIPIENS: ALLELE REPLACEMENT AND CHANGING ENVIRONMENT

Fixation of adaptive mutations in populations is often constrained by pleiotropic fitness costs. The evolutionary pathways that compensate such fitness disadvantages are either the occurrence of modifier genes or replacement of the adaptive allele by less costly ones. In this context, 23 years of evolution of insecticide resistance genes in the mosquito Culex pipiens from southern France are analyzed. The aim of this study is to answer the following points. Is there a fitness cost associated with these resistance genes in natural populations? Does evolution proceed through allele replacement or through selection of modifiers? And finally, how do environmental changes affect the evolution of resistance genes? Samples from the same transect, crossing the boundary between an insecticide‐treated and a nontreated area, are analyzed. Clinal analyses indicate a variable fitness cost among the resistance genes and show that allele replacement has been the primary mechanism of resistance evolution in this area. It is also shown that replacement was probably due to environmental changes corresponding to modification in pesticide‐treatment intensity.

Pleiotropy of adaptive changes in populations: comparisons among insecticide resistance genes in Culex pipiens

Resistance to toxicants is a convenient model for investigating whether adaptive changes are associated with pleiotropic fitness costs. Despite the voluminous literature devoted to this subject, intraspecific comparisons among toxicant resistance genes are rare. We report here results on the pleiotropic effect on adult survival of Culex pipiens mutants involved in the same adaptation: the resistance to organophosphorus insecticides. This field study was performed in southern France where four resistance genes sequentially appeared and increased in frequency in response to intense insecticide control. By repeated sampling of overwintering females through winter, we analysed the impact of each of three resistance genes on adult survival. We showed that (i) the most recent gene seems to be of no disadvantage during winter, (ii) the oldest affects survival in some environmental conditions, and (iii) the third induces a constant, severe and dominant survival cost. Such variability is discussed in relation to the physiological changes involved in resistance.

Host race formation in the Acari

Host race formation generates diversity within species and may even lead to speciation. This phenomenon could be particularly prevalent in the Acari due to the often intimate interaction these species have with their hosts. In this review, we explore the process of host race formation, whether it is likely to occur in this group and what features may favour its evolution. Although few studies are currently available and tend to be biased toward two model species, results suggest that host races are indeed common in this group, and more likely to occur when hosts are long-lived. We discuss future directions for research on host-associated adaptations in this group of organisms and the potential relevance of host race formation for the biodiversity of mites and ticks.

Changing distributions of ticks: causes and consequences.

Today, we are witnessing changes in the spatial distribution and abundance of many species, including ticks and their associated pathogens. Evidence that these changes are primarily due to climate change, habitat modifications, and the globalisation of human activities are accumulating. Changes in the distribution of ticks and their invasion into new regions can have numerous consequences including modifications in their ecological characteristics and those of endemic species, impacts on the dynamics of local host populations and the emergence of human and livestock disease. Here, we review the principal causes for distributional shifts in tick populations and their consequences in terms of the ecological attributes of the species in question (i.e. phenotypic and genetic responses), pathogen transmission and disease epidemiology. We also describe different methodological approaches currently used to assess and predict such changes and their consequences. We finish with a discussion of new research avenues to develop in order to improve our understanding of these host–vector–pathogen interactions in the context of a changing world.

Modelling the spatial configuration of refuges for a sustainable control of pests: a case study of Bt cotton

Abstract The ‘high‐dose‐refuge’ (HDR) strategy is widely recommended by the biotechnology industry and regulatory authorities to delay pest adaptation to transgenic crops that produce Bacillus thuringiensis (Bt) toxins. This involves cultivating nontoxic plants (refuges) in close proximity to crops producing a high dose of Bt toxin. The principal cost associated with this strategy is due to yield losses suffered by farmers growing unprotected, refuge plants. Using a population genetic model of selection in a spatially heterogeneous environment, we show the existence of an optimal spatial configuration of refuges that could prevent the evolution of resistance whilst reducing the use of costly refuges. In particular, the sustainable control of pests is achievable with the use of more aggregated distributions of nontransgenic plants and transgenic plants producing lower doses of toxin. The HDR strategy is thus suboptimal within the context of sustainable agricultural development.