Lingering effects of childhood: Larval ecology impacts vector-parasite-host interactions

Background/Question/Methods

For organisms with complex life cycles, ecological interactions and abiotic factors acting on larval stages can have profound effects on adult population dynamics and adult physiology. Resource competition among immature stages, in particular can: prolong development; increase larval mortality; and reduce adult size, fecundity, and longevity.  For insect vectors of pathogens, competition among larvae sometimes enhances adult infection susceptibility to arthropod-borne viruses and malaria, with a greater proportion of adults from density-stressed larval environments becoming physiologically competent vectors of disease. However, competition among larvae probably also affects body condition and longevity, which may alter the fitness costs of infection, and could reduce probability of density-stressed adults surviving, contacting vertebrate hosts, and transmitting the pathogen via a blood meal. Determining these opposing impacts upon vector physiology may be vital for understanding the role of larval ecology in modifying vector-parasite-host interactions and ultimately, disease transmission. We tested the relationship between Aedes aegypti larval rearing density and its susceptibility to infection by, and ability to act as vector for the nematode Brugia pahangi. We postulated that competition among larvae would modify fitness costs of parasitism. 

Results/Conclusions

Competitively stressed mosquitoes had a greater parasite load and greater mean number of mature B. pahangi in the head (i.e., greater vector competence), which is consistent with past studies showing that density stress on larvae enhances adult vector competence.  Adult vector mortality was positively related to microfilarial titer of the experimental vertebrate host (Meriones unguiculatus) regardless of larval rearing conditions. Mosquitoes reared at high density had significantly greater post-infection mortality, and those that survived to dissection (days 8-12 post-infection) displayed significantly reduced ability to fly, effectively inhibiting host finding. These results suggest that larval competition alters fitness effects of B. pahangi on the vector, consistent with hypotheses of a competition-mediated tradeoff between larval growth and development vs. adult tolerance of infection. Contrary to previous studies, our results imply that mosquitoes from benign larval rearing environments are more physiologically and ecologically capable vectors of B. pahangi.  Results from this laboratory model system suggest that testing for complex density-mediated effects on natural vector-pathogen-host systems could reveal important aspects of disease ecology.