Life history interactions with environmental conditions in a host–parasite relationship and the parasite's mode of transmission

Abstract

The microsporidian parasite Edhazardia aedis is capable of vertical or horizontal transmission among individuals of its host, the mosquito Aedes aegypti, and either mode of transmission may follow the other. We show that following the horizontal infection of host larvae, the parasite's subsequent mode of transmission largely depends on host life history traits and their responses to different environmental conditions. In two experiments the intensity of larval exposure to infection and the amount of food available to them were simultaneously manipulated. One experiment followed the dynamics of host development and the parasite's production of spores while the other estimated the outcome of their relationship. Host life history traits varied widely across treatment conditions while those of the parasite did not. Of particular importance was the host's larval growth rate. Horizontal rather than vertical transmission by the parasite was more likely as low food and high dose conditions favoured slower larval growth rates. This pattern of transmission behaviour with host growth rate can be considered in terms of reproductive value: the potential vertical transmission success that female mosquitoes offer the parasite decreases as larval growth rates slow and makes them more attractive to exploitation for horizontal transmission (requiring host mortality). However, the lack of variation in the parasite's life history traits gave rise in some conditions to low estimates for both its vertical and horizontal transmission success. We suggest that the unresponsive behaviour of the parasite's life history traits reflects a bet-hedging strategy to reduce variance in its overall transmission success in the unpredictable environmental conditions and host larval growth rates that this parasite encounters in nature.