Dynamics of the "popcorn" Wolbachia infection in outbred Aedes aegypti informs prospects for mosquito vector control

Abstract

Forty percent of the world's population is at risk of contracting dengue virus, which produces dengue fever with a potentially fatal hemorrhagic form. The wMelPop Wolbachia infection of Drosophila melanogaster reduces life span and interferes with viral transmission when introduced into the mosquito Aedes aegypti, the primary vector of dengue virus. Wolbachia has been proposed as an agent for preventing transmission of dengue virus. Population invasion by Wolbachia depends on levels of cytoplasmic incompatibility, fitness effects, and maternal transmission. Here we characterized these traits in an outbred genetic background of a potential target population of Ae. aegypti using two crossing schemes. Cytoplasmic incompatibility was strong in this background, and the maternal transmission rate of Wolbachia was high. The infection substantially reduced longevity of infected adult females, regardless of whether adults came from larvae cultured under high or low levels of nutrition or density. The infection reduced the viability of diapausing and nondiapausing eggs. Viability was particularly low when eggs were laid by older females and when diapausing eggs had been stored for a few weeks. The infection affected mosquito larval development time and adult body size under different larval nutrition levels and densities. The results were used to assess the potential for wMelPop-CLA to invade natural populations of Ae. aegypti and to develop recommendations for the maintenance of fitness in infected mosquitoes that need to compete against field insects.

Figure 1.—

Crossing schemes for developing outbred lines of Aedes aegypti carrying the wMelPop-CLA infection. The schemes are shown for the C1 mass-bred line (crossed in the third generation from the field) and equivalent crosses were carried out for the C2 mass-bred line to generate four outcrossed lines (AOC1, AOC2, BOC1, and BOC2). In Scheme A, the mass-bred line was crossed to the infected O line (35 generations after introduction of wMelPop-CLA) and then backcrossed to the mass-bred line maintained in culture. In Scheme B, the mass-bred line was put in diapause and resurrected for each generation of backcrossing to minimize laboratory adaptation.

Figure 2.—

Effect of Wolbachia infection on survival of Aedes aegypti females from the outbred lines when held in groups. Lines reflect the average survival of two replicates from each scheme.

Figure 3.—

Change in hatch rate of eggs of Aedes aegypti with number of days of treatment at three temperatures. Humidities were combined in these graphs because of the weak effects detected for humidity in the analyses (see Table 1). Error bars represent standard errors.

Figure 4.—

Changes in hatch rate of Aedes aegypti in compatible and incompatible crosses in C1 lines with females of different ages.

Figure 5.—

Adult life span of male (A) and female (B) Aedes aegypti reared under varying larval nutrition and densities. Shaded lines, infected AOC1 line; solid lines, uninfected C1 line.