Environmental factors influence the local establishment of Wolbachia in Aedes aegypti mosquitoes in two small communities in central Vietnam

Hiển, Nguyễn Trần; Anh, Đặng Đức; Le, Nguyen H.; Yen, Nguyen T.; Phong, Trần Vũ; Nam, Vũ Sinh; Dương, Trần Như; Nguyen, Nguyen B.; Huong, Duong T.T.; Hung, Luu Q.; Trinh, Chau N.T.; Hoàng, Nguyễn Viết; Vien, Quang Mai; Nghia, Le Trung; Đông, Nguyễn Thành; Tho, Le Huu; Kutcher, Simon; Hurst, Tim; Montgomery, Jacqui; Woolfit, Megan; Rancès, Edwige; Kyrylos, Peter; Anders, Katherine L.; Nguyen, Le; Brown-Kenyon, Jack; Caird, Angela; McLean, Breeanna J.; Iturbe‐Ormaetxe, Iñaki; Ritchie, Scott A.; O'Neill, Scott Leslie; Ryan, Peter

doi:10.12688/gatesopenres.13347.2

Cited by 19 publications

(25 citation statements)

References 50 publications

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“…aegypti into two small communities in Nha Trang City in central Vietnam resulted in a seasonal heterogeneity of w Mel invasion and spread into the local Ae . aegypti populations with a reduced prevalence of Wolbachia infection in mosquitoes during the hot dry season, followed by an increased prevalence during the cooler season, and such seasonal variation in Wolbachia infection prevalence in mosquitoes was associated with elevated temperature and was possibly due to imperfect maternal transmission of Wolbachia [ 36 ]. These studies suggested that the maternal transmission of the two Wolbachia strains can become unstable in Ae.…”

Section: Discussionmentioning

confidence: 99%

Sensitivity of wMel and wAlbB Wolbachia infections in Aedes aegypti Puducherry (Indian) strains to heat stress during larval development

et al. 2022

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Background ICMR-Vector Control Research Centre, Puducherry, India, developed two colonies of Aedes aegypti infected with wMel and wAlbB Wolbacia strains called Ae. aegypti (Pud) lines for dengue control. The sensitivity of wMel and wAlbB strains in Ae. aegypti (Pud) lines to heat stress was studied. Methods wMel and wAlbB infected and uninfected Ae. aegypti larvae (first to fourth instars) were reared in the laboratory to adults at 26 °C, 30 °C, 36 °C and 40 °C constant temperatures and also 26–30 °C, 26–36 °C and 26–40 °C diurnal cyclic temperatures. The adults were tested for Wolbachia infection. Experiments were also carried out rearing the larvae under simulated field conditions in summer (April and June) under sunlight using fully open and half open bowls and also under sunlight and natural shade. Results At 36 °C and 40 °C constant temperatures, complete larval mortality was observed. At 30 °C and 26 °C, no larval mortality occurred, but Wolbachia density was relatively low in wMel infected males compared to control (maintained at 26 ± 1 °C). At diurnal cyclic temperature of 26–40 °C, Wolbachia density was reduced in males of both the (Pud) lines, but not in females. At 26–36 °C, reduction in Wolbachia density was observed in wMel males but not in wAlbB males. At 26–30 °C, no significant reduction in Wolbachia density was observed with wMel and wAlbB strains. In simulated field conditions (April), under sunlight, the daytime water temperature reached a maximum of 35.7 °C in both full and half open bowls. No larval mortality occurred. Wolbachia frequency and density was reduced in wMel-infected Ae. aegypti (Pud) males from both type of bowls and in females from full open bowls, and in wAlbB males from half open bowls. In June, rearing of larvae under sunlight, the first-instar larvae experienced a maximum daytime water temperature of > 38 °C that caused complete mortality. No larval mortality was observed in bowls kept under shade (< 32 °C). Conclusions Exposure of larvae to higher rearing temperatures in the laboratory and simulated-field conditions reduced the densities of wMel and wAlbB strains particularly in males, but the impact was more pronounced for wMel strain. The actual effect of heat stress on the stability of these two Wolbachia strains needs to be tested under natural field conditions. Graphical Abstract

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Section: Discussionmentioning

confidence: 99%

Sensitivity of wMel and wAlbB Wolbachia infections in Aedes aegypti Puducherry (Indian) strains to heat stress during larval development

et al. 2022

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“…aegypti for population replacement is now underway in 11 countries to evaluate its effectiveness in controlling dengue (World Mosquito Program [WMP], 2022). This strain has successfully been established in Australia (O'Neill et al, 2018;Ryan et al, 2020), Brazil (Pinto et al, 2021), Indonesia (Utarini et al, 2021), and Vietnam (Hien et al, 2022), while wAlbB was successfully established among wild mosquito population in Malaysia for population replacement (Nazni et al, 2019). In a recent randomized control trial in Yogyakarta city, Indonesia, field releases of wMel-infected Ae.…”

Section: Introductionmentioning

confidence: 99%

Studies on the fitness characteristics of wMel- and wAlbB-introgressed Aedes aegypti (Pud) lines in comparison with wMel- and wAlbB-transinfected Aedes aegypti (Aus) and wild-type Aedes aegypti (Pud) lines

Sadanandane

Gunasekaran²,

Devaraju³

et al. 2022

Front. Microbiol.

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Wolbachia, an intracellular maternally transmitted endosymbiont, has been shown to interfere with the replication of dengue virus in Aedes aegypti mosquitoes. The Wolbachia-transinfected Ae. aegypti has been currently released in many countries to test its effectiveness in preventing the transmission of dengue virus. ICMR-Vector Control Research Centre in collaboration with World Mosquito Program Monash University, Australia, has generated two new Wolbachia-introgressed Ae. aegypti Puducherry (Pud) lines via backcrossing Ae. aegypti females of Australian (Aus) strains, infected with wMel and wAlbB Wolbachia with wild-type Ae. aegypti Puducherry (Pud) males. Wolbachia infections are known to induce a fitness cost and confer benefit on the host mosquito populations that will influence spread of the Wolbachia into native wild mosquito populations during the field release. Hence, the induced fitness cost or benefit/advantage in the two newly generated Ae. aegypti (Pud) lines was assessed in the laboratory in comparison with the wild-type Ae. aegypti (Pud) strain. In addition, maternal transmission (MT) efficiency, induced cytoplasmic incompatibility (CI), and insecticide resistance status of the two (Pud) lines were determined to assess the likely frequency of wMel and wAlbB infections in the native wild population after field invasion. The study shows that wMel and wAlbB infections did not induce any fitness cost on the two newly generated (Pud) lines. Rather, in terms of wing length, fecundity, egg hatch rate, and adult survival, the Wolbachia introgression conferred fitness benefits on the (Pud) lines compared to uninfected Wolbachia free wild Ae. aegypti population. wMel and wAlbB exhibited a high maternal transmission (99–100%) and induced nearly complete (98–100%) cytoplasmic incompatibility. Both the (Pud) lines were resistant to deltamethrin, malathion, DDT, and temephos, and the level of resistance was almost the same between the two lines as in the wild type. Overall, the stable association of wMel and wAlbB established with Ae. aegypti and the reproductive advantages of the (Pud) lines encourage a pilot release in the field for population replacement potential.

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“…Recent studies have shown that w AlbB is more stable at high temperature than w Mel in Ae. aegypti , leading to the proposed release of w AlbB in areas where it is challenging for w Mel to establish infection because of its high susceptibility to extreme summer temperatures and wide yearly temperature ranges ( 41–43 ). Based on analysis of the w AlbB whole-genome sequence, only four single nucleotide variants have occurred over 15 years of transinfection ( 43 ).…”

Section: Introductionmentioning

confidence: 99%

Wolbachia wAlbB remains stable in Aedes aegypti over 15 years but exhibits genetic background-dependent variation in virus blocking

et al. 2022

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The ability of the maternally transmitted endosymbiotic bacterium Wolbachia to induce cytoplasmic incompatibility (CI) and virus blocking makes it a promising weapon for combatting mosquito-borne diseases through either suppression or replacement of wild-type populations. Recent field trials show that both approaches significantly reduce the incidence of dengue fever in humans. However, new questions emerge about how Wolbachia-mosquito associations will co-evolve over time and whether Wolbachia-mediated virus blocking will be affected by the genetic diversity of mosquitoes and arboviruses in the real world. Here, we have compared the Wolbachia density and CI expression of two wAlbB-infected Aedes aegypti lines transinfected 15 years apart. We have also assessed wAlbB-mediated virus blocking against dengue (DENV), Zika (ZIKV), and Chikungunya (CHIKV) viruses and examined whether host genetic backgrounds modulate viral blocking effects by comparing ZIKV infection in mosquitoes with a Mexican genetic background to those with a Singaporean background. Our results show that over 15 years, wAlbB maintained the capacity to form a stable association with Ae. aegypti in terms of both density and CI expression. There were variations in wAlbB-induced virus blocking against CHIKV, DENV, and ZIKV, and higher inhibitory effects on ZIKV in mosquitoes on the Singaporean genetic background than on the Mexican background. These results provide important information concerning the robustness and long-term stability of Wolbachia as a biocontrol agent for arbovirus disease control.

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Environmental factors influence the local establishment of Wolbachia in Aedes aegypti mosquitoes in two small communities in central Vietnam

Cited by 19 publications

References 50 publications

Sensitivity of wMel and wAlbB Wolbachia infections in Aedes aegypti Puducherry (Indian) strains to heat stress during larval development

Sensitivity of wMel and wAlbB Wolbachia infections in Aedes aegypti Puducherry (Indian) strains to heat stress during larval development

Studies on the fitness characteristics of wMel- and wAlbB-introgressed Aedes aegypti (Pud) lines in comparison with wMel- and wAlbB-transinfected Aedes aegypti (Aus) and wild-type Aedes aegypti (Pud) lines

Wolbachia wAlbB remains stable in Aedes aegypti over 15 years but exhibits genetic background-dependent variation in virus blocking

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