Larval competition alters susceptibility of adult Aedes mosquitoes to dengue infection

Abstract

Dengue, the most important human arboviral disease, is transmitted primarily by Aedes aegypti and, to a lesser extent, by Aedes albopictus. The current distributions of these invasive species overlap and are affected by interspecific larval competition in their container habitats. Here we report that competition also enhances dengue infection and dissemination rates in one of these two vector species. We determined the effects of competition on adult A. aegypti and A. albopictus, comparing their susceptibility to infection with a Southeast Asian strain of dengue-2 virus. High levels of intra- or interspecific competition among larvae enhanced the susceptibility of A. albopictus to dengue virus infection and potential for transmission, as indicated by disseminated infections. Doubling the number of competing larvae (A. albopictus or A. aegypti), led to a significant (more than 60%) increase in the proportion of A. albopictus with disseminated dengue-2 infection. Competition-enhanced vector competence appears to result from a reduction in 'barriers' (morphological or physiological) to virus infection and dissemination and may contribute to the importance of A. albopictus in dengue transmission. Similar results for other unrelated arboviruses suggest that larval competition, common in mosquitoes, should be considered in estimates of vector competence for pathogens that infect humans.

Figure 1

Bivariate plot of least square (LS) means (±s.e.) for A. albopictus and A. aegypti female size and time to emergence. Competition treatments consisted of numbers of A. albopictus : A. aegypti per container—160 : 0 (open circle), 320 : 0 (filled circle), 160 : 160 (grey circle and grey square), 0 : 320 (filled square) and 0 : 160 (open square). Different lower- and uppercase letters indicate significant differences between bivariate means for A. albopictus and A. aegypti, respectively. Aedes albopictus are represented by circles and A. aegypti by squares.

Figure 2

Least square (LS) means (±s.e.) for estimated finite rate of increase, λ′, for A. albopictus (filled circles) and A. aegypti (open squares). Points without bars have standard errors too small to be visible. Different lower- and uppercase letters indicate significant differences between means for A. albopictus and A. aegypti, respectively.

Figure 3

Bivariate plot of least square (LS) means (±s.e.) for proportion of Aedes females infected and proportion with disseminated infections after fed on a dengue-2 virus (Southeast Asian strain 16803) blood meal. Competition treatments consisted of numbers of A. albopictus : A. aegypti per container—160 : 0 (open circle), 320 : 0 (filled circle), 160 : 160 (grey circle and grey square), 0 : 320 (filled square) and 0 : 160 (open square)—as treatments. Different lower- and uppercase letters indicate significant differences between bivariate means for A. albopictus and A. aegypti, respectively. Aedes albopictus are represented by circles and A. aegypti by squares.