Mosquitoes do senesce: departure from the paradigm of constant mortality

Abstract

Although variation in mortality is considered by virtually all vector-borne disease specialists to be one of the most important determinants of an arthropod's capacity to transmit pathogens, the operational assumption often is that insect vector mortality is independent of age. Acceptance of the non-senescence assumption leads to the erroneous conclusion that mosquito age is unimportant, results in misleading predictions regarding disease reductions after vector control, and represses study of other aspects of mosquito biology that change with age. We brought large-scale laboratory life table techniques (N > 100,000) to bear on the question of age-dependent mortality in the mosquito vector of dengue virus, Aedes aegypti. Mortality was highly age dependent in both sexes. Mortality was low at young ages (< 10 days old), steadily increased at middle ages, and decelerated at older ages. A newly derived age-dependent model of pathogen transmission shows the importance of young mosquitoes and population age structure to transmission dynamics. Departure from the age-independent mortality paradigm encourages research on overlooked complexities in mosquito biology, the need for innovative methods to study mosquito population dynamics, and the need to study age-dependent changes for an accurate understanding of mosquito biology and pathogen transmission.

FIGURE 1

Smoothed hazard rate of 45,054 female and 55,997 male sucrose-fed Ae. aegypti housed in 29 cages (thin black lines). Thick red lines designate mean hazard rates for each sex. Hazard curves were derived and smoothed using local least squares regression. Hazard curves were cut off at the point when 10 females or 10 males remained alive in each cage.

FIGURE 2

Parameter values of best-fit mortality models for 29 cohorts of sugar-fed males (○) and females (●). All female cohorts and all but one cohort of males (best fit by Gompertz model, marked with an *) were best fit by a logistic or logistic-Makeham mortality model. Parameter values include initial mortality rate (a), rate of exponential increase (b), rate of mortality deceleration (s), and a constant term (c). Mortality models (Gompertz, Gompertz-Makeham, logistic, and logistic-Makeham.) were fit to the observed mortality data by WinModest 1.0.

FIGURE 3

Smoothed hazard rate of female Ae. aegypti fed human blood (N = 187; dashed line), human blood plus 10% sucrose (N = 188; gray line), or 10% sucrose (N = 197; black line). Each line represents the combined data from two cohorts. Mortality curves were smoothed using a running geometric mean (width = 7).

FIGURE 4

Vectorial capacity of mosquitoes at the age when first biting an infectious host (age-specific vectorial capacity). Mosquitoes exhibited one of four mortality patterns: exponential (♦), Gompertz (○), logistic (▲), or mean mortality from large-scale study (*). The number of mosquitoes in each age class is held constant for this simulation.

FIGURE 5

Vectorial capacity contributed by each age class of mosquito based on the age when they first bite an infectious host. Populations exhibited either synchronous emergence or stable age distribution age structures. Four mortality patterns were used: exponential (♦), Gompertz (○), logistic (▲), and mean mortality from large-scale study (*). Inset, Total population vectorial capacity (C_t) for each model/age structure combination and percent difference from mortality data from large-scale study.