Malaria control and senescence: the importance of accounting for the pace and shape of aging in wild mosquitoes

Abstract

The assumption that vector mortality remains constant with age is used widely to assess malaria transmission risk and predict the public health consequences of vector control strategies. However, laboratory studies commonly demonstrate clear evidence of senescence, or a decrease in physiological function and increase in vector mortality rate with age. Despite recognition of its importance, practical limitations have stifled definitive observations of mosquito senescence in the wild, where rates of extrinsic mortality are much higher than those observed under protected laboratory conditions. We developed methods to integrate available field data to understand mortality in wild Anopheles gambiae, the most import vector of malaria in sub-Saharan Africa. We found evidence for an increase in rates of mortality with age. As expected, we also found that overall mortality is far greater in wild cohorts than commonly observed under protected laboratory conditions. The magnitude of senescence increases with An. gambiae lifespan, implying that most wild mosquitoes die long before cohorts can exhibit strong senescence. We reviewed available published mortality studies of Anopheles spp. to confirm this fundamental prediction of aging in wild populations. Senescence becomes most apparent in long-living mosquito cohorts; cohorts with low extrinsic mortality, such as protected laboratory cohorts, suffer a relatively high proportion of senescent deaths. Imprecision in estimates of vector mortality and changes in mortality with age will severely bias models of vector borne disease transmission risk, such as malaria, and the sensitivity of transmission to bias increases as the extrinsic incubation period of the parasite decreases. While we focus here on malaria, we caution that future transmission models of anti-vectorial interventions must incorporate both realistic mortality rates and age-dependent changes in mortality.

Mosquito species and age influence thermal performance of traits relevant to malaria transmission

“…The temperature-sensitive age-dependent mortality rates for mosquito populations are concordant with previous work in laboratory and limited field studies (51, 73, 74). While there is some evidence that long-lived An.…”

“…stephensi . Thus, whether mosquitoes experience senescence in the field remains an open and critical question, primarily due to the logistical difficulties of accurately aging mosquitoes, conducting mark-recapture studies, and controlling for temperature in variable environments (51).…”

“…This could have important ramifications for predicting mosquito population dynamics as well as the effectiveness of mosquito control interventions in the field where thermal conditions vary. Further, imprecise estimates of lifespan can have a compounding effect on predictions of population dynamics and vector-borne disease transmission as it impacts estimates of total reproductive output and the amount of time a mosquito survives past becoming infectious (51, 52, 77). More effort is needed in measuring both lifespan and age-associated changes in life history traits under field settings for important mosquito disease vectors.…”

The importance of temperature fluctuations in understanding mosquito population dynamics and malaria risk

“…Given the importance of mosquito age structure to malaria risk, further development and testing of new age-grading techniques under field conditions would be beneficial for understanding vector populations and ground-truthing our models. Additionally, there is evidence that age-dependent mortality may be important for understanding disease risk [52,53]; it would therefore be useful to explore the effects of age-dependent mortality on temporal variation in age structure.…”

Global expansion and redistribution of Aedes-borne virus transmission risk with climate change

“…The data used to fit the mechanistic models are derived from dengue virus traits in mosquitoes from multiple source populations from independently-published trait thermal response studies [6]. In addition, many of the traits are measured in laboratory strains and rearing conditions, which may distort life-history relative to wild vector populations, although this will be more problematic for pathogens with longer development times, such as malaria [68]. For Ae.…”