AbstractEcological conditions may greatly affect the relative importance of vertical and horizontal transmission, in particular for parasites with a mixed mode of transmission. Resource availability is one important environmental factor, affecting host growth and fecundity, but also the parasite’s own development. The consequences for the potential of vertical and horizontal transmission and for the evolution of transmission mode are largely unknown. We let the mixed-mode microsporidian parasite Edhazardia aedis evolve on its mosquito host Aedes aegypti under high-food or low-food conditions, representing permissive and restricted conditions. These alter the timing of development of infected larvae and thereby the probabilities for the parasites to enter the vertical or horizontal transmission pathways. After 10 generations, evolved parasites were assayed under the two food levels. There was an ecological trade-off between transmission modes, mediated by nutrient effects on host development, resulting in a higher vertical transmission (VT) potential under high-food and a higher horizontal transmission (HT) potential under low-food test conditions. Evolution under high food increased the VT potential of the parasite, particularly if it was tested at low food. This involved higher probability of carrying binucleate spores for the emerging females, greater fecundity and a longer life compared to parasites that were tested in the same conditions but had evolved under low food. The changes are related to the developmental regulation and switch in the production of two spore types, affecting investment in VT or HT. In contrast, the HT potential remained relatively unaffected by the parasite’s evolutionary history, suggesting that, within our experiential design, the VT mode evolved independently of the HT mode. Our work illustrates the possible links between resource availability, within-host developmental processes and the evolution of parasite transmission investment. Future work, theoretical and experimental, should scale up from within-host to between-host levels, including eco-evolutionary and epidemiological dynamics.