Abstract

Two hypotheses for how conditions for larval mosquitoes affect vectorial capacity make opposite predictions about the relationship of adult size and frequency of infection with vector-borne pathogens. Competition among larvae produces small adult females. The competition-susceptibility hypothesis postulates that small females are more susceptible to infection and predicts frequency of infection should decrease with size. The competition-longevity hypothesis postulates that small females have lower longevity and lower probability of becoming competent to transmit the pathogen and thus predicts frequency of infection should increase with size. We tested these hypotheses for Aedes aegypti in Rio de Janeiro, Brazil, during a dengue outbreak. In the laboratory, longevity increases with size, then decreases at the largest sizes. For field-collected females, generalised linear mixed model comparisons showed that a model with a linear increase of frequency of dengue with size produced the best Akaike’s information criterion with a correction for small sample sizes (AICc). Consensus prediction of three competing models indicated that frequency of infection increases monotonically with female size, consistent with the competition-longevity hypothesis. Site frequency of infection was not significantly related to site mean size of females. Thus, our data indicate that uncrowded, low competition conditions for larvae produce the females that are most likely to be important vectors of dengue. More generally, ecological conditions, particularly crowding and intraspecific competition among larvae, are likely to affect vector-borne pathogen transmission in nature, in this case via effects on longevity of resulting adults. Heterogeneity among individual vectors in likelihood of infection is a generally important outcome of ecological conditions impacting vectors as larvae.

Highlights

  • Epidemic dengue, which evolved in modern times from a sylvatic zoonosis to direct mosquito-human transmission through adaptation to peridomestic Aedes spp vectors (Moncayo et al 2004), is currently the most prevalent arboviral disease affecting humans

  • The two hypotheses for effects of competition on dengue transmission yield two different predicted relationships between frequency of dengue infection and female body size: the competition-susceptibility hypothesis predicts that frequency of infection should decrease as body size increases; in contrast, the competition-longevity hypothesis predicts that frequency of infection should increase as body size increases, assuming larger females have greater lifespan

  • Part two is a test of the relationship of frequency of dengue infection to female size among females collected in neighbourhoods of Rio de Janeiro during the 2008 dengue outbreak, controlling for both time and location of collection

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Summary

Introduction

Epidemic dengue, which evolved in modern times from a sylvatic zoonosis to direct mosquito-human transmission through adaptation to peridomestic Aedes spp vectors (Moncayo et al 2004), is currently the most prevalent arboviral disease affecting humans Larval competition in laboratory microcosms significantly increased the susceptibility of the vector Aedes albopictus to experimental infection with dengue virus (DENV) and potential transmission (Alto et al 2008a) In both Aedes aegypti and Ae. albopictus, adult female body size, which covaries with both larval rearing temperature and competition intensity, was negatively correlated with dengue infection rates in laboratory studies (Alto et al 2008b). On the other hand greater competition among larvae produces small adult females with shorter adult lifespans, rendering them less likely to live long enough both to acquire the infection and to become competent to pass the infection on during subsequent blood meals (competitionlongevity hypothesis) Though these hypotheses are not mutually exclusive, we can ask the question: which postulated effect of competition among larvae is most important in natural transmission of DENV?. Part two is a test of the relationship of frequency of dengue infection to female size among females collected in neighbourhoods of Rio de Janeiro during the 2008 dengue outbreak, controlling for both time and location of collection

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