Temperature‐sensitive fitness cost of insecticide resistance in Chinese populations of the diamondback moth Plutella xylostella

Abstract

Alleles conferring a higher adaptive value in one environment may have a detrimental impact on fitness in another environment. Alleles conferring resistance to pesticides and drugs provide textbook examples of this trade-off as, in addition to conferring resistance to these molecules, they frequently decrease fitness in pesticide/drug-free environments. We show here that resistance to chlorpyrifos, an organophosphate (OP), in Chinese populations of the diamondback moth, Plutella xylostella, is conferred by two mutations of ace1 - the gene encoding the acetylcholinesterase enzyme targeted by OPs - affecting the amino acid sequence of the corresponding protein. These mutations were always linked, consistent with the segregation of a single resistance allele, ace1R, carrying both mutations, in the populations studied. We monitored the frequency of ace1R (by genotyping more than 20 000 adults) and the level of resistance (through bioassays on more than 50 000 individuals) over several generations. We found that the ace1R resistance allele was costly in the absence of insecticide and that this cost was likely recessive. This fitness costs involved a decrease in fecundity: females from resistant strains laid 20% fewer eggs, on average, than females from susceptible strains. Finally, we found that the fitness costs associated with the ace1R allele were greater at high temperatures. At least two life history traits were involved: longevity and fecundity. The relative longevity of resistant individuals was affected only at high temperatures and the relative fecundity of resistant females - which was already affected at temperatures optimal for development - decreased further at high temperatures. The implications of these findings for resistance management are discussed.

Fitness costs and life table parameters of highly insecticide‐resistant strains of Plutella xylostella (L.) (Lepidoptera: Plutellidae) at different temperatures

“…The fitness costs resulting from insecticide resistance are more or less dependent on environmental factors that have a great impact on life history traits; in particular, when the environment is unfavourable for insect development the estimated costs tend to be high. Environmental stressors such as high or low temperatures, parasitism and food quality were shown to have a negative effect on developmental time, fertility and mortality, thereby limiting population growth. Moreover, negative genetic trade‐offs can also be apparent in the absence of the insecticide or in the presence of sublethal doses .…”

“…Zhang et al . investigated the temperature effects on organophosphate (OP)‐resistant DBM strains and concluded that extremely cold or warm conditions are unfavourable for insect development and may also modify the fitness costs associated with pesticide resistance.…”

“…Here, we investigated the effect of temperature on the fitness of three resistant strains of P. xylostella in comparison with a susceptible reference strain. Generally, it is well known that alleles that confer a higher adaptive value in one environment may have a negative impact on fitness in another environment . Therefore, our aim was to evaluate changes in the overall fitness, including development, fecundity, mortality and population growth parameters, as fitness costs might be involved in DBM resistance against insecticides and rather apparent at higher or lower temperature than optimum temperatures.…”

“…14 On the other hand, fitness costs can also be absent, as seen in the housefly, Musca domestica, where a fitness advantage was observed for kdr mutatation in the voltage-gated sodium channel. 15 Zhang et al 5 investigated the temperature effects on organophosphate (OP)-resistant DBM strains and concluded that extremely cold or warm conditions are unfavourable for insect development and may also modify the fitness costs associated with pesticide resistance. They found that the fitness costs associated with the ace1R allele which is causing OP resistance were greater at high temperatures.…”

“…Generally, it is well known that alleles that confer a higher adaptive value in one environment may have a negative impact on fitness in another environment. 5 Therefore, our aim was to evaluate changes in the overall fitness, including development, fecundity, mortality and population growth parameters, as fitness costs might be involved in DBM resistance against insecticides and rather apparent at higher or lower temperature than optimum temperatures. Furthermore, this study contributes to the understanding of fitness costs in relation to different resistance traits present in DBM and how they possibly can affect the population under applied conditions.…”