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.
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.
Two ecotypes have been described for Culex pipiens mosquitoes of the temperate zone: a human commensal type and a feral type, but their degree of evolutionary differentiation and taxonomic status are still unclear. The commensal form is characterized by life-history traits probably adaptive to underground man-made environments. This situation has sometimes been considered as an example of recent speciation although the existence of intermediate forms indicates that the balance between gene flow and disruptive selection should first be assessed. The present study was concerned with (1) the determination of biological traits involved in adaptation to commensalism, and (2) the pattern of gene flow within and between ecotypes in a restricted area. It was found that (1) significant differences in biological traits exist between mosquitoes from different habitats, (2) characteristics of the commensal type are not universal in mosquitoes from underground manmade habitats, (3) allozyme markers do not clearly differentiate ecotypes and (4) insecticide resistance genes, which reveal recent migration, occur in each ecotype. These results are discussed in the context of possible speciation due to commensalism.
Abstract.-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.
In some insect species, knockdown resistance (kdr) to pyrethroids and DDT is linked to point mutations in the sequence of the para‐type voltage‐dependent sodium channel gene. The effects of pyrethroids were assayed on six Culex pipiens strains: two were susceptible to pyrethroids and the four others displayed various levels of resistance, but, in each case, a kdr‐type mechanism was strongly suggested. Degenerate primers were designed on the basis of the corresponding sequences of the para orthologous gene reported from several orders of insects. These primers were used to amplify the region of the sodium channel gene which includes the positions where the kdr and super‐kdr mutations have been found in Musca domestica. As expected, the amplified fragment was highly homologous to the para sequences. The super‐kdr‐like mutation (methionine to threonine at position 918 of the M domestica para sequence) was never detected in any strain. In contrast, the same kdr mutation (leucine to phenylalanine at position 1014) was present in some Culex pyrethroid‐resistant samples. An alternative substitution of the same leucine to a serine was detected in one strain slightly resistant to pyrethroids but highly resistant to DDT. These data have allowed us to design a PCR‐based diagnostic test on genomic DNA to determine the presence or the absence of the kdr allele in single C pipiens collected in several countries. The validity of this test was checked by comparing the frequency of the resistance allele and the toxicological data. © 1999 Society of Chemical Industry
SummaryWe have investigated the distribution of resistance genes in relation to genetic structure and gene flow between various islands of French Polynesia in Culex pipiens quinquefasciatus. We show that (1) resistance to organophosphorous insecticides, mediated by A2–B2 esterases, is present in all islands, (2) A2–B2 frequency decreases as distance from Tahiti increases, and (3) genetic differentiation (measured as estimates of the Fst, parameter from allozyme polymorphism) between islands is significantly correlated to geographic distances which is also correlated to air or sea commercial traffic. These data are discussed in relation to A2–B2 invasion of French Polynesian islands.
Within the Llobregat Delta (Barcelona, Spain), Culex pipiens L. has been the target of organophosphate insecticide (OP) control for 10 yr (1982-1992). Between 1991 and 1992, OPs were replaced by Bacillus-based toxins in all the mosquito control programs within > 150 km of this area. The distribution of several OP-resistance genes was surveyed within the Llobregat Delta and neighboring populations (< 25 km) during the 2 yr following this regional pesticide change to investigate how the change in selection pressure affected the dynamics of OP-resistance genes. The immigration failure of the A2-B2 resistant esterases and the observed difference in OP-resistance dynamics between isolated and nonisolated populations may indicate fitness disadvantages associated with OP-resistance genes, hence a tendency for a decrease in OP-resistance. In contrast, one OP-resistance gene further increased in frequency, whereas the frequencies of some others were maintained. These unexpected results question the importance of pesticides from sources other than mosquito control, and the variability of pleiotropic fitness costs among pesticide resistance genes.
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