Effect of Larval Competition on Extrinsic Incubation Period and Vectorial Capacity of Aedes albopictus for Dengue Virus

Abstract

Despite the growing awareness that larval competition can influence adult mosquito life history traits including susceptibility to pathogens, the net effect of larval competition on human risk of exposure to mosquito-borne pathogens remains poorly understood. We examined how intraspecific larval competition affects dengue-2 virus (DENV-2) extrinsic incubation period and vectorial capacity of its natural vector Aedes albopictus. Adult Ae. albopictus from low and high-larval density conditions were orally challenged with DENV-2 and then assayed for virus infection and dissemination rates following a 6, 9, or 12-day incubation period using real-time quantitative reverse transcription PCR. We then modeled the effect of larval competition on vectorial capacity using parameter estimates obtained from peer-reviewed field and laboratory studies. Larval competition resulted in significantly longer development times, lower emergence rates, and smaller adults, but did not significantly affect the extrinsic incubation period of DENV-2 in Ae. albopictus. Our vectorial capacity models suggest that the effect of larval competition on adult mosquito longevity likely has a greater influence on vectorial capacity relative to any competition-induced changes in vector competence. Furthermore, we found that large increases in the viral dissemination rate may be necessary to compensate for small competition-induced reductions in daily survivorship. Our results indicate that mosquito populations that experience stress from larval competition are likely to have a reduced vectorial capacity, even when susceptibility to pathogens is enhanced.

Fig 1. Effect of larval competition on Aedes albopictus life history traits.

Panel A displays the effect of larval density on emergence rate. Panel B presents a bivariate plot of female time to emergence and female wing length. Error bars represent the standard errors of the mean. Tests of significance were corrected for multiple comparisons using the Tukey-Kramer adjustment. Bivariate means followed by different lower—and uppercase letters indicate significant differences in wing length and time to emergence respectively.

Fig 2. Ae. albopictus body and disseminated leg infection rates.

Panel A-C shows the body infection rate by larval density, incubation period, and larval density by incubation period respectively. Panel D-F shows the disseminated infection rate by larval density, incubation period and larval density by incubation period. Bars above and below the means represent the standard errors of the mean. For each panel, estimates with a different letter are significantly different at P = 0.05, after controlling for multiple comparisons using the Tukey-Kramer adjustment.

Fig 3. Effect of larval density (A), incubation period (B) and larval density by incubation period (C) on DENV titer in infected mosquito bodies.

Bars above and below the means represent the standard errors of the mean. For each panel, estimates with a different letter are significantly different at P = 0.05, after controlling for multiple comparisons using the Tukey-Kramer adjustment.

Fig 4. Effect of larval competition on vectorial capacity.

Panel A displays the vectorial capacity values for high and low density treatments at the 6, 9, and 12-day incubation periods. Panel B displays the cumulative vectorial capacity for high and low-density treatments. Tests of significance were corrected for multiple comparisons using the Tukey-Kramer adjustment. Different letters indicate significant differences in means.

Fig 5. Cumulative vectorial capacity of high and low density treatments across a range of human biting rates.

Fig 6. Change in viral dissemination rate necessary to compensate for decrease in daily survivorship rate.

The figure above displays the change in viral dissemination rate necessary to compensate for a reduction in the daily survivorship rate by the specified amount from an estimated 90% survival rate.