The pattern of kdr mutations correlated with the temperature in field populations of Aedes albopictus in China

Abstract

Background Aedes albopictus is the primary vector of dengue fever in China. This mosquito species has a wide distribution range in China and can be found in the tropical climate zones of southern provinces through to temperate climate zones of northern provinces. Insecticides are an important control method, especially during outbreaks of dengue fever, but increasing insecticide resistance raises the risk of failure to control vector-borne diseases. Knockdown resistance (kdr) caused by point mutations in the voltage-gated sodium channel (VGSC) gene is a key mechanism that confers resistance to pyrethroids. In this study we explored the characteristics and possible evolutionary trend of kdr mutation in Ae. albopictus based on analysis of the kdr mutations in field populations of mosquitoes in China. Methods A total of 1549 adult Ae. albopictus were collected from 18 sites in China from 2017 to 2019 and 50 individuals from three sites in the 1990s. A fragment of approximately 350 bp from part of the S6 segment in the VGSC gene domain III was amplified and sequenced. Using TCS software version 1.21A, we constructed haplotypes of the VGSC gene network and calculated outgroup probability of the haplotypes. Data of annual average temperatures (AAT) of the collection sites were acquired from the national database. The correlation between AAT of the collection site and the kdr mutation rate was analyzed by Pearson correlation using SPSS software version 21.0. Results The overall frequency of mutant allele F1534 was 45.6%. Nine mutant alleles were detected at codon 1534 in 15 field populations, namely TCC/TCG (S) (38.9%), TTG/CTG/CTC/TTA (L) (3.7%), TGC (C) (2.9%), CGC (R) (0.3%) and TGG (W) (0.1%). Only one mutant allele, ACC (T), was found at codon 1532, with a frequency of 6.4% in ten field populations. Moreover, multiple mutations at alleles I1532 and F1534 in a sample appeared in five populations. The 1534 mutation rate was significantly positively related to AAT (Pearson correlation: r(18) = 0.624, P = 0.0056), while the 1532 mutation rate was significantly negatively related to AAT (Pearson correlation: r(18) = − 0.645, P = 0.0038). Thirteen haplotypes were inferred, in which six mutant haplotypes were formed by one step, and one additional mutation formed the other six haplotypes. In the samples from the 1990s, no mutant allele was detected at codon 1532 of the VGSC gene. However, F1534S/TCC was found in HNHK94 with an unexpected frequency of 100%. Conclusions Kdr mutations are widespread in the field populations of Ae. albopictus in China. Two novel mutant alleles, F1534W/TGG and F1534R/CGC, were detected in this study. The 1534 kdr mutation appeared in the population of Ae. albopictus no later than the 1990s. The F1534 mutation rate was positively correlated with AAT, while the I1532 mutation rate was negatively correlated with AAT. These results indicate that iInsecticide usage should be carefully managed to slow down the spread of highly resistant Ae. albopictus populations, especially in the areas with higher AAT. Graphical abstract

Population genetic structure of Aedes albopictus (Diptera: Culicidae) in China inferred by microsatellite and association with knockdown resistance mutations

“…The high allelic diversity and expected heterozygosity were observed in most of the populations (H O = 0.32-0.57), which was similar to the level of diversity in the Ae. albopictus of the coastal areas in southern China (H O = 0.384-0.641) [23], and 17 populations from 3 climatic regions of China (H O = 0.467-0.627) [ Notably, the F ST value of GDST population was minimum (0.087), meanwhile carrying no mutation in F1534 [34]. As the collection site is close to the seaside wharf, therefore it was speculated that GDST population mosquito was imported from ships and colonized locally.…”

“…albopictus in China and signi cantly associated with pyrethroid resistance phenotype [54]. The frequency of F1534S was obtained from our published literature [34], which populations were the same as the theses samples. Pearson correlation coe cient R was used to examine the association between the two variables and was calculated by SPSS 20.0 (IBM Corp., Armonk, NY, USA).…”

“…In our previous study, we found that the kdr mutation pattern of Ae. albopictus population in China was correlated with the average annual temperature at the collection site [34]. Gao et al showed that Ae.…”

Knockdown resistance mutations distribution and characteristics of Aedes albopictus field populations within eleven dengue local epidemic provinces in China

“…Previous studies state that temperature is the most important ecological factor affecting the physiology of Aedes species, in addition to the gonotrophic cycle length and the survival rate of adults (Brady et al, 2014). Chen et al (Chen et al, 2021) analyzed the correlation between annual average temperature, and kdr mutations, indicating that temperature possibly affects insecticide resistance. In addition, it has been reported that multiple loci mutations in the VGSC gene can simultaneously increase the level of resistance (Plernsub et al, 2016).…”

Geographic distribution of the V1016G knockdown resistance mutation in Aedes albopictus: a warning bell for Europe

“…Despite studies having so far mostly focused on major vector species, in the last decade a few mutations within the vssc gene have also been identified in Ae. albopictus, in particular in positions 1534 (F1534C/S/L/W/R; [19,[33][34][35][36]), 1016 (V1016G/I [34,36,37]) and 1532 (I1532T [38]). Among these, the only alleles confirmed to be associated with strong pyrethroid resistance phenotypes are 1534C [37], 1534S [18,36,37,39] and 1016G [29,37].…”