Differences in Longevity and Temperature-Driven Extrinsic Incubation Period Correlate with Varying Dengue Risk in the Arizona-Sonora Desert Region

Abstract

Dengue transmission is determined by a complex set of interactions between the environment, Aedes aegypti mosquitoes, dengue viruses, and humans. Emergence in new geographic areas can be unpredictable, with some regions having established mosquito populations for decades without locally acquired transmission. Key factors such as mosquito longevity, temperature-driven extrinsic incubation period (EIP), and vector-human contact can strongly influence the potential for disease transmission. To assess how these factors interact at the edge of the geographical range of dengue virus transmission, we conducted mosquito sampling in multiple urban areas located throughout the Arizona-Sonora desert region during the summer rainy seasons from 2013 to 2015. Mosquito population age structure, reflecting mosquito survivorship, was measured using a combination of parity analysis and relative gene expression of an age-related gene, SCP-1. Bloodmeal analysis was conducted on field collected blood-fed mosquitoes. Site-specific temperature was used to estimate the EIP, and this predicted EIP combined with mosquito age were combined to estimate the abundance of "potential" vectors (i.e., mosquitoes old enough to survive the EIP). Comparisons were made across cities by month and year. The dengue endemic cities Hermosillo and Ciudad Obregon, both in the state of Sonora, Mexico, had higher abundance of potential vectors than non-endemic Nogales, Sonora, Mexico. Interestingly, Tucson, Arizona consistently had a higher estimated abundance of potential vectors than dengue endemic regions of Sonora, Mexico. There were no observed city-level differences in species composition of blood meals. Combined, these data offer insights into the critical factors required for dengue transmission at the ecological edge of the mosquito's range. However, further research is needed to integrate an understanding of how social and additional environmental factors constrain and enhance dengue transmission in emerging regions.

Keywords: Aedes aegypti; Mexico; age-grading; climate; dengue; extrinsic incubation period; longevity; mosquito; parity.

Figure 1

Map of study cities in the Arizona-Sonora Desert region from Arizona (USA) to Sonora (Mexico).

Figure 2

Ct Ratio and Age relationship. The RNA extraction protocol was changed after the initial Joy et al. 2012 paper [26] to eliminate problems caused by extraction from mosquito abdomens. New thresholds were identified (and used in Ernst et al. 2017 [27]): Ct ratio ≥ 1.92: ≤ 5 days old; 0.78 ≤ Ct ratio < 1.92: 6–14 days old; Ct ratio < 0.78: > 14 days old. The new regression model is shown above, with mosquitoes colored by their feeding status. The best-fit linear regression model is shown (bold black line): log(age)~rcs(Ct ratio, 3), where rcs represents a restricted cubic spline with three knots. Fed and non-fed mosquitoes did not differ significantly in their expression profiles (p = 0.313; Wald test of regression coefficient for feeding status).

Figure 3

Extrinsic Incubation Period and Temperature model: To account for study-level effects, a mixed effects model was run with random intercepts by study and a 6-knot restricted cubic spline for temperature. The predicted EIP values for the data points used to construct that model were then entered as data in a separate OLS mixed effects model, again with a 6-knot restricted cubic spline for temperature and log transformation of EIP. This model is identical to the previous model in terms of mean estimates, though standard errors are different. The value of this model is in eliminating intra-study variability to visualize average effects estimated by each study.

Figure 4

Average female mosquito trap catches by city and sampling period (early = 15 July to 14 August; mid = 15 August to 14 September; late = 15 September to 14 October) for years 2013 to 2015. An asterisk * denotes a city with mosquito counts that are significantly different (p < 0.05) from the reference city, Hermosillo (in yellow).

Figure 5

Proportion of parous mosquitoes by city and year. The asterisk * denotes cities with significantly different parity levels (p < 0.05) than the reference city, Hermosillo (in light blue).

Figure 6

Bloodmeal analysis conducted on engorged female Ae. aegypti mosquitoes from trapping events in Tucson, AZ, Hermosillo, SN, and Heroica Nogales, SN from 2013–2015. The proportion of mosquitoes found with blood of each mammalian species. No significant differences by city. 2014 had significantly less human bloodmeals than the other years.