Amplification of DNA from preserved specimens shows blowflies were preadapted for the rapid evolution of insecticide resistance

Abstract

Mutations of esterase 3 confer two forms of organophosphate resistance on contemporary Australasian Lucilia cuprina. One form, called diazinon resistance, is slightly more effective against commonly used insecticides and is now more prevalent than the other form, called malathion resistance. We report here that the single amino acid replacement associated with diazinon resistance and two replacements associated with malathion resistance also occur in esterase 3 in the sibling species Lucilia sericata, suggesting convergent evolution around a finite set of resistance options. We also find parallels between the species in the geographic distributions of the polymorphisms: In both cases, the diazinon-resistance change is absent or rare outside Australasia where insecticide pressure is lower, whereas the changes associated with malathion resistance are widespread. Furthermore, PCR analysis of pinned specimens of Australasian L. cuprina collected before the release of organophosphate insecticides reveals no cases of the diazinonresistance change but several cases of those associated with malathion resistance. Thus, the early outbreak of resistance in this species can be explained by the preexistence of mutant alleles encoding malathion resistance. The pinned specimen analysis also shows much higher genetic diversity at the locus before organophosphate use, suggesting that the subsequent sweep of diazinon resistance in Australasia has compromised the scope for the locus to respond further to the ongoing challenge of the insecticides.Lucilia cuprina ͉ Lucilia sericata ͉ mutation ͉ convergent evolution ͉ organophosphates O ne of the major unresolved issues in our understanding of adaptive evolutionary change is the extent to which the acquisition of newly beneficial traits proceeds by the selection of existing (preadaptive) rare variants, rather than waiting on new mutations to arise once the selection pressure is imposed. These two scenarios could have very different consequences for the nature of the acquired adaptation, its rate of uptake, and the fate of genetic variation in the chromosomal region surrounding the selected locus. Direct evidence discriminating the two possibilities in natural populations of eukaryotes has been lacking because the critical data needed must include samples that have not been exposed to the selection pressure.The phenomenon of insecticide resistance is proving an informative model for studying microevolutionary processes in eukaryotes because it represents a rapid contemporary acquisition of a major new biochemical phenotype and it generally has a relatively simple genetic basis. The rapidity with which resistance often follows the first use of new pesticides has prompted much speculation about preadaptation at the relevant loci (1, 2). However, many cases have also been recorded where resistant genotypes have fitness costs in the absence of insecticide (3, 4), which would seem at odds with the preadaptation hypothesis. In this paper, we present evidence that tests the hypothesis direct...

Fitness costs of key point mutations that underlie acaricide target‐site resistance in the two‐spotted spider miteTetranychus urticae

“…In light of this theory, the study of the potential biological weaknesses that are associated with acaricide/insecticide resistance in populations is of high importance in the context of Insecticide Resistance Management (IRM; Crow, 1957; Georghiou & Taylor, 1977). The origin and history of the nucleotide polymorphisms associated with resistance remains largely unknown (but see Gould et al., 1997; Hartley et al., 2006), which lowers the reliability of a priori predictions of potential fitness costs. In this study, we took advantage of a collection of near‐isogenic lines to quantify potential pleiotropic fitness effects of five key mutations associated with resistance in T. urticae .…”

Key questions in the genetics and genomics of eco-evolutionary dynamics

“…Interestingly, this evidence often comes from some of the same systems and traits that were discussed above, including Pitx1 in stickleback, lactose tolerance in some human populations (Tishkoff et al, 2007), diazinon resistance in blowflies (Hartley et al, 2006), acetylcholinesterase resistance in Drosophila (Karasov et al, 2010) and local adaptation in Arabidopsis (Hancock et al, 2011). These studies suggest that new mutations can be important even when populations contain lots of standing variation, although not necessarily for the same traits.…”

“…Application to natural populations often yields a similar conclusion, with examples including lactose tolerance in humans (Myles et al, 2005), warfarin resistance in brown rats (Rattus norvegicus) (Pelz et al, 2005), malathion resistance in blowflies (Lucilia spp.) (Hartley et al, 2006), local adaptation in Arabidopsis thaliana (Fournier-Level et al, 2011), and several traits in stickleback (Colosimo et al, 2005;Miller et al, 2007;Kitano et al, 2008;Jones et al, 2012b). Of particular relevance, the evolutionary changes observed in many of these cases took place over relatively short time frames (decades to centuries).…”

The Molecular Genetics of Insecticide Resistance

“…This topic has also been recently discussed more extensively elsewhere (ffrench-Constant 2007), but it is worth noting that our knowledge about the molecular basis of resistance has facilitated a "forensic" approach to this problem. Thus the ability to amplify resistance-associated genes from historical pinned specimens of the Australian sheep blowfly allowed Hartley et al (2006) to show that the mutations conferring resistance to malathion (but not to diazinon) were already present in 21 pinned specimens collected before the introduction of the organophosphorus insecticides themselves. This finding is of interest first because it suggests first that resistance-associated mutations that appear before their associated insecticide may have had some other function prior to their role in resistance.…”