Global temperature constraints on Aedes aegypti and Ae. albopictus persistence and competence for dengue virus transmission

Abstract

Background: Dengue is a disease that has undergone significant expansion over the past hundred years. Understanding what factors limit the distribution of transmission can be used to predict current and future limits to further dengue expansion. While not the only factor, temperature plays an important role in defining these limits. Previous attempts to analyse the effect of temperature on the geographic distribution of dengue have not considered its dynamic intra-annual and diurnal change and its cumulative effects on mosquito and virus populations.

Methods: Here we expand an existing modelling framework with new temperature-based relationships to model an index proportional to the basic reproductive number of the dengue virus. This model framework is combined with high spatial and temporal resolution global temperature data to model the effects of temperature on Aedes aegypti and Ae. albopictus persistence and competence for dengue virus transmission.

Results: Our model predicted areas where temperature is not expected to permit transmission and/or Aedes persistence throughout the year. By reanalysing existing experimental data our analysis indicates that Ae. albopictus, often considered a minor vector of dengue, has comparable rates of virus dissemination to its primary vector, Ae. aegypti, and when the longer lifespan of Ae. albopictus is considered its competence for dengue virus transmission far exceeds that of Ae. aegypti.

Conclusions: These results can be used to analyse the effects of temperature and other contributing factors on the expansion of dengue or its Aedes vectors. Our finding that Ae. albopictus has a greater capacity for dengue transmission than Ae. aegypti is contrary to current explanations for the comparative rarity of dengue transmission in established Ae. albopictus populations. This suggests that the limited capacity of Ae. albopictus to transmit DENV is more dependent on its ecology than vector competence. The recommendations, which we explicitly outlined here, point to clear targets for entomological investigation.

Figure 1

Rate of incubation in Ae. aegypti (blue) and Ae. albopictus (orange). The data from each individual assay are shown by blue triangles for Ae. aegypti (n = 373) and orange circles for Ae. albopictus (n = 125). The fitted lines for rate of EIP completion for each experiment are shown in faded blue lines for Ae. aegypti and faded orange lines for Ae. alboipictus. The mean fit for each species is shown in thick solid blue (Ae. aegypti) and orange/brown (Ae. albopictus) lines. The black dotted line indicates the point at which 50% of the population will have completed incubation, which is equivilent to the mean EIP.

Figure 2

Relationship between temperature and length of the first gonotrophic cycle for Ae. aegypti and Ae. albopictus. The bold line shows the predicted mean first gonotrophic cycle length and the shaded areas show the prediction standard deviation for Ae. aegypti (blue) and Ae. albopictus (red).

Figure 3

Ae. aegypti temperature suitability for persistence and DENV transmission. (A) The annualised summary of temperature suitability for oviposition (X_ovi(T)) on a normalised scale. (B) Introduction suitability; the number of days in a year where introduction of a DENV infected human would lead to ongoing transmission (Z(T)_i > 0). (C) Persistence suitability; the number of days in the year where onward DENV transmission could occur if a constant source of infectious humans were available (X(T)_i > 0). (D) The annualised summary of temperature suitability (X(T)) on a normalised scale. Predictions in all above maps are constrained to areas that permit oviposition (X_ovi(T)_i > 0) on 219 or more days in the year, as determined by comparison with known occurrences of Ae.aegypti.

Figure 4

Ae. albopictus temperature suitability for persistence and DENV transmission. Panels correspond directly to those described for Ae. aegypti in Figure 3, but constraints are expanded to areas that permit oviposition for 365 days in the year.

Figure 5

Comparative temperature suitability of Ae. aegypti (A) and Ae. albopictus (B). The annualised temperature suitability index (X(T)) normalised relative to the maximum value of both species and plotted on a logarithmic scale.