Impact of temperature on dengue and chikungunya transmission by the mosquito Aedes albopictus

Abstract

The mosquito Aedes albopictus is an invasive species first detected in Europe in Albania in 1979, and now established in 28 European countries. Temperature is a limiting factor in mosquito activities and in the transmission of associated arboviruses namely chikungunya (CHIKV) and dengue (DENV). Since 2007, local transmissions of CHIKV and DENV have been reported in mainland Europe, mainly in South Europe. Thus, the critical question is how far north transmission could occur. In this context, the Albanian infestation by Ae. albopictus is of interest because the species is present up to 1200 m of altitude; this allows using altitude as a proxy for latitude. Here we show that Ae. albopictus can transmit CHIKV at 28 °C as well as 20 °C, however, the transmission of DENV is only observed at 28 °C. We conclude that if temperature is the key environmental factor limiting transmission, then transmission of CHIKV, but not DENV is feasible in much of Europe.

Figure 1

PCoA plot obtained from the F_STP matrix using GenAlEx (a) and graphical representation of the co-ancestry percentages obtained with Distruct 1.1. (b). In panel (a), highlighted populations are those showing a higher genetic correlation. In panel (b), each cluster is represented by a specific color and each bar represents a specific individual and its percentage of identity to the two clusters (K1 and K2).

Figure 2

Dissemination and transmission efficiencies of Ae. albopictus populations infected with CHIKV examined at different days (3, 7, 10, 14, and 21) after incubation at different temperatures (20 °C, 20 °C variable, 28 °C). After infection, mosquito heads and saliva were titrated. (a) Dissemination efficiency corresponds to the proportion of mosquitoes with infected heads. (b) Transmission efficiency refers to the proportion of mosquitoes with infectious saliva. Error bars show the exact Binomial confidence interval (95%).

Figure 3

Predicted value of Dissemination Efficiency (DE, panel a) and Transmission Efficiency (TE, panel b) according to days-post infection, modeled using logistic regression. In both panels, graphs show the expected marginal means (dots) with corresponding 95% confidence intervals (bars) on the logit scale, highlighting the interacting effect of temperature on days post-infection.

Figure 4

Viral titers in saliva of Ae. albopictus infected with CHIKV and examined at different days (3 (a,f,k), 7 (b,g,l), 10 (c,h,m), 14 (d,l,n), and 21(e,j,o)) after incubation at different temperatures (20 °C, 20 °C variable, 28 °C). Saliva was collected from individual females using the forced salivation technique and titrated on C6/36 Ae. albopictus cells. Bars indicate the mean.

Figure 5

Dissemination and transmission efficiencies of Ae. albopictus populations infected with DENV examined at different days (3, 7, 10, 14, and 21) after incubation at different temperatures (20 °C, 20 °C variable, 28 °C). After infection, mosquito heads and saliva were titrated. (a) Dissemination efficiency corresponds to the proportion of mosquitoes with infected heads. (b) Transmission efficiency refers to the proportion of mosquitoes with infectious saliva. Error bars show the exact Binomial confidence interval (95%).

Figure 6

Aedes albopictus populations collected in Albania. Mosquitoes were processed for genotyping with microsatellites and vector competence studies to DENV and CHIKV. The figure was prepared by Eng. Migel Ali, GIS expert at the Company Geo Consulting Albania (https://gc-al.com/en/staff_mali.php).