Fitness cost in field and laboratory Aedes aegypti populations associated with resistance to the insecticide temephos

Abstract

Background: The continued use of chemical insecticides in the context of the National Program of Dengue Control in Brazil has generated a high selective pressure on the natural populations of Aedes aegypti, leading to their resistance to these compounds in the field. Fitness costs have been described as adaptive consequences of resistance. This study evaluated the biological and reproductive performance of A. aegypti strains and a field population resistant to temephos, the main larvicide used for controlling mosquitoes.

Methods: Comparative tests were performed with a resistant field population from the municipality of Arcoverde, Pernambuco State, Brazil, with a high rate of temephos resistance (RR = 226.6) and three isogenetic laboratory strains from the same origin (Araripina municipality, Pernambuco): RecR (RR = 283.6); RecRNEx (RR = 250.5), a strain under a process of resistance reversion; and RecRev (RR = 2.32), a reversed susceptible strain used as an experimental control.

Results: Our study revealed that the absence of selective pressure imposed by exposure to temephos, for five consecutive generations, led to a discrete reduction of the resistance ratio and the response of the detoxifying enzymes. Most of the 19 biological parameters were impaired in the resistant strains and field population. The analysis of the fertility life table confirmed the presence of reproductive disadvantages for the resistant individuals. Similarly, the longevity, body size, and total energetic resources were also lower for the resistant females, except for the last two parameters in the field females (Arcoverde). In contrast, the sex ratio and embryonic viability suffered no interference in all strains or population evaluated, regardless of their status of resistance to temephos.

Conclusions: The reproductive potential and survival of the resistant individuals were compromised. The parameters most affected were the larval development time, fecundity, net reproduction rate, and the generational doubling time. These fitness costs in the natural population and laboratory strains investigated are likely associated with maintaining the metabolic mechanism of resistance to temephos. Our results show that despite these costs, the highly temephos resistant populations can compensate for these losses and successfully overcome the control actions that are based on the use of chemical insecticides.

Fig. 1

Profile of enzymes related to the detoxification of chemical insecticides in the Aedes aegypti laboratory strains and the field population. Alfa-Esterase (α-Est), Beta-Esterase (β-Est), PNPA-esterase (PNPA), Glutathione-S-transferase (GST) and mixed-function oxidases (MFO). The bar indicates the frequency of individuals with altered enzyme activities in the following populations: a) RecReverse; b) RecRNEx; c) RecR and d) Arcoverde. The green bar represents population considered normal (when the frequency of mosquitoes with altered enzymatic activity was <15 %), the yellow bar represents population considered altered (when the frequency of mosquitoes with altered enzymatic activities was between 15 and 50 %), and the red bar represents population considered highly altered (frequency of mosquitoes with the altered enzymatic activity >50 %)

Fig. 2

Size and shape analysis of the Aedes aegypti females from three strains and the field population through geometric morphometrics of wings. a) global isometric sizes (in pixels) of the A. aegypti wings with distinctive susceptibility profiles to temephos: RecRev (Susceptible), RecRNEx (resistant non-exposed), RecR (Resistant exposed), and Arcoverde (Resistant field). R: right wing; L: left wing. The central lines show the original means, and the intervals represent the standard error (± SE). b) Scatter plot of A. aegypti females showing three different clusters: 1) Arcoverde (red); 2) RecRNEx and RecR (purple and green, respectively); and 3) RecRev (blue). Clustering is measured by the canonical variate analysis, which takes into account the shape and size of female wings

Fig. 3

Reproductive parameters and longevity of Aedes aegypti females from different strains and the field population. a) fecundity (average number of eggs per female); b) fertility (average number of L_1/number of eggs/female) c) longevity (average time in days); Columns followed by the same symbol do not differ significantly from each other by Tukey’s test (p < 0.0005)

Fig. 4

Percent of egg viability of Aedes aegypti strains and the field population according to the quiescence time (0–180 days). The lines represent the hatching rate (%) in eggs with different times of quiescence: 0 days; 30 days; 60 days; 90 days; 120 days; 150 days; and 180 days. There was no statistically significant difference between groups