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.