Co-occurrence of viruses and mosquitoes at the vectors’ optimal climate range: An underestimated risk to temperate regions?

<div><p>Mosquito-borne viruses have been estimated to cause over 100 million cases of human disease annually. Many methodologies have been developed to help identify areas most at risk from transmission of these viruses. However, generally, these methodologies focus predominantly on the effects of climate on either the vectors or the pathogens they spread, and do not consider the dynamic interaction between the optimal conditions for both vector and virus. Here, we use a new approach that considers the complex interplay between the optimal temperature for virus transmission, and the optimal climate for the mosquito vectors. Using published geolocated data we identified temperature and rainfall ranges in which a number of mosquito vectors have been observed to co-occur with West Nile virus, dengue virus or chikungunya virus. We then investigated whether the optimal climate for co-occurrence of vector and virus varies between “warmer” and “cooler” adapted vectors for the same virus. We found that different mosquito vectors co-occur with the same virus at different temperatures, despite significant overlap in vector temperature ranges. Specifically, we found that co-occurrence correlates with the optimal climatic conditions for the respective vector; cooler-adapted mosquitoes tend to co-occur with the same virus in cooler conditions than their warmer-adapted counterparts. We conclude that mosquitoes appear to be most able to transmit virus in the mosquitoes’ optimal climate range, and hypothesise that this may be due to proportionally over-extended vector longevity, and other increased fitness attributes, within this optimal range. These results suggest that the threat posed by vector-competent mosquito species indigenous to temperate regions may have been underestimated, whilst the threat arising from invasive tropical vectors moving to cooler temperate regions may be overestimated.</p></div

Optimal mosquito season for sub-countries.

<p>Maps showing A: the period of the OMS as defined by the model parameters described in the methods; B the mean temperature of this season. Areas coloured in grey have insufficient data for this analysis.</p

Transmission risk of two example mosquito species.

<p>Despite significant overlap in temperature envelopes (red boxes), Species 1 (Sp 1) is more cold-adapted than Species 2 (Sp 2) and its envelope extends further into colder temperatures, and less far into warm temperatures. In scenario 1, the optimum temperature for virus transmission (shown as white line against grey shading) is the same for both Sp 1 and Sp 2, despite the different temperature envelopes of the vectors. Our hypothesis corresponds to scenario 2, where the optimum temperature for virus transmission is lower for cooler-adapted Sp 1, and higher for warmer-adapted Sp 2.</p

Mating competitiveness of Uju.wMel males.

<p>Competitiveness of Uju.wMel males was assessed using three independent replicates of 50 male Uju.wMel : 50 male Uju.wt (<i>w</i>AlbA/B) : 50 females of either Uju.wMel or Uju.wt (total of 300 females in six cages). Hatching embryos indicated a compatible cross where both male and female parents were infected with the same <i>Wolbachia</i>. Error bars show the SEM. No significant differences in male mating competitiveness were found between the two lines with Chi-squared analysis using a likelihood framework.</p

Vector mean OMS temperatures.

<p>Vector mean OMS temperatures.</p

CHIKV challenge.

<p>Mosquitoes were allowed to feed on artificial blood meals containing virus suspension and 7 days post infection 35–50 females were used for forced salivation. Samples were titrated by focus fluorescent assay on <i>Ae. albopictus</i> C6/36 cells. The transmission rate was estimated as the percentage of mosquitoes with infectious saliva among tested mosquitoes (A). Saliva samples were titrated by focus fluorescent assay on C6/36 <i>Ae. albopictus</i> cell culture. The total number of plaques was counted and the titer was calculated as FFU/saliva (B). No significant difference was found between Uju.wt and UjuT viral titers using a Wilcoxon rank sum test.</p

Diagram of the hypothesized effect of temperature on longevity.

<p>Longevity of three example mosquito species, each adapted to a different (low, medium and high) mean temperature. As temperature increases, the longevity of all mosquitoes is decreased (top panels). However, here we hypothesize that mosquito species adapted to cooler temperatures will live proportionally longer than will warmer-adapted species in these cooler temperatures and less long in the warmer temperatures (compare top panels). At a given temperature, as longevity increases so does the potential number of infectious bites the vector can make. Consequently, mosquitoes adapted to a particular temperature, will have the highest vectorial capacity at the respective temperature (bottom panels).</p

Hatch rate and fecundity of Uju.wMel.

<p>Egg hatch (A) and fecundity or mean number of eggs produced per female per gonotrophic cycle (B) of Uju.wMel was assessed at generation sixteen. Females were blood fed at six days post eclosion, individualized for laying, and eggs hatched after five days. Second instar larvae were counted to calculate percent hatch (A) and eggs per batch per female counted to give fecundity (B). A: Uju.wMel n = 452, UjuT n = 858, Uju.wt n = 508. B: Uju.wMel n = 16, UjuT n = 14, Uju.wt n = 20. Error bars represent the SEM.</p

Known and potential vectors of West Nile virus, chikungunya virus and dengue virus listed in the EID2 database.

<p>Known and potential vectors of West Nile virus, chikungunya virus and dengue virus listed in the EID2 database.</p

Temperature ranges of vectors and vector/virus co-occurrence.

<p>Kernel density estimations for the density of the different mosquitoes across their temperature ranges. The green area represents all single vector sub-countries, whilst the red area represents the density of sub-countries in which the relevant virus was also found. For single vector sub countries with or without virus/ single vector sub countries with virus only: chikungunya virus (<i>Ae</i>. <i>aegypti</i> n = 112/24, <i>Ae</i>. <i>albopictus</i> n = 48/9), dengue virus (<i>Ae</i>. aegypti n = 117/73, <i>Ae</i>. <i>albopictus</i> n = 48/24); West Nile virus (<i>Ae</i>. <i>vexans</i> n = 12/5, <i>C</i>. <i>pipiens</i> n = 63/25, <i>C</i>. <i>quinquefasciatus</i> n = 46/9). Grey ticks beneath the graph represent the actual OMS temperature of each of the sub-countries (with or without virus) described by the graph. Note: values of <i>n</i> for the same vector species but different viruses vary as a result of different lists of vector species resulting in different numbers of single-vector sub-countries.</p