Rapid evolution of knockdown resistance haplotypes in response to pyrethroid selection in Aedes aegypti.

Jennifer Baltzegar,Fred Stell,Michael Fisher,Thomas W Scott,Fred Gould,Audrey Lenhart,Gissella Vasquez,Helvio Astete,Christian Gunning,Alun L Lloyd,Michael Vella,Amy Morrison

doi:10.1111/eva.13269

Abstract

This study describes the evolution of knockdown resistance (kdr) haplotypes in Aedes aegypti in response to pyrethroid insecticide use over the course of 18 years in Iquitos, Peru. Based on the duration and intensiveness of sampling (~10,000 samples), this is the most thorough study of kdr population genetics in Ae. aegypti to date within a city. We provide evidence for the direct connection between programmatic citywide pyrethroid spraying and the increase in frequency of specific kdr haplotypes by identifying two evolutionary events in the population. The relatively high selection coefficients, even under infrequent insecticide pressure, emphasize how quickly Ae. aegypti populations can evolve. In our examination of the literature on mosquitoes and other insect pests, we could find no cases where a pest evolved so quickly to so few exposures to low or nonresidual insecticide applications. The observed rapid increase in frequency of resistance alleles might have been aided by the incomplete dominance of resistance‐conferring alleles over corresponding susceptibility alleles. In addition to dramatic temporal shifts, spatial suppression experiments reveal that genetic heterogeneity existed not only at the citywide scale, but also on a very fine scale within the city.

Highlights

The mosquito Aedes aegypti (L.) transmits yellow fever, dengue, Zika, and chikungunya viruses
The selection coefficient (s) and dominance (h) of the resistance allele were estimated at each locus in the population for the periods when each resistance allele was increasing in frequency by following the Wright–Fisher approximate Bayesian computation (WFABC) method for temporally sampled data (Foll et al, 2014)
We examined the temporal and spatial patterns of kdr alleles in Ae. aegypti from Iquitos, Peru, across an 18-year period (2000–2017)

Summary

| INTRODUCTION

The mosquito Aedes aegypti (L.) transmits yellow fever, dengue, Zika, and chikungunya viruses. In Central and South America, pyrethroid resistance in Ae. aegypti has been associated with single nucleotide mutations that cause amino acid changes from valine (V) to isoleucine (I) at position 1016 (V1016I) and from phenylalanine (F) to cysteine (C) at position 1534 (F1534C) (numbered according to homology in the house fly, Musca domestica) in the VGSC protein (Table 1) (Deming et al, 2016; Linss et al, 2014). Peru, is a well-established study site for Ae. aegypti and dengue in the Western Hemisphere with a long history of entomological research and sampling that can help elucidate the factors contributing to pyrethroid resistance evolution in this mosquito We examined the temporal and spatial patterns of kdr allele frequencies in Ae. aegypti over 18 years (~180–216 generations) in Iquitos, Peru This timeframe (2000–2017) spanned years prior, during, and after citywide use of pyrethroids for mosquito control. The dominance and selection coefficients of the resistance alleles were anticipated to affect the rate that resistance haplotypes increased in frequency in the population

| MATERIALS AND METHODS

| DISCUSSION

Findings

| CONCLUSION