Evolutionary ecology of vector-parasite interactions

Abstract

Ecological interactions between parasites and their within-host environment and within-vector environment (in the case of vector-borne diseases) shape the severity and transmission of infections. Therefore, applying evolutionary ecology frameworks to explain how and why parasites respond to environmental variation is becoming increasingly more common. A greater understanding of within-host and within-vector ecology can improve predictions of parasite evolution in response to disease control interventions and other environmental changes. Malaria is the deadliest vector-borne disease and is caused by parasites of the Plasmodium genus which are transmitted between vertebrate hosts via mosquitoes (often Anopheles spp.). However, despite its public health importance and decades of intensive research, fundamental aspects of malaria transmission remain poorly understood. In particular, the sources of variation in parasite life history traits that shape within-vector development and onward transmission to a new vertebrate host have received little attention.

By integrating evolutionary ecology, parasitology and vector biology, I investigate how environmentally determined variation in vector traits shapes parasite traits expressed within the vector, and the subsequent implications for between-host transmission and parasite evolutionary potential. It is becoming increasingly important to understand how parasites evolve to cope with the challenges and/or exploit the opportunities provided by their within-vector environment, because vector control tools are altering vector genotypes and phenotypes. Therefore, I firstly created a framework using evolutionary ecology to predict how parasites could evolve in response to vector control tool-imposed changes in their vectors, collating the consequences of these changes into overarching agents of selection acting on parasites (Chapter 2). Following this, I focussed on the following key aspects that arose, examining: (i) whether genetic variation within parasite populations influences the potential for selection to act on fitness-related traits (Chapter 3), (ii) the extent of plasticity for parasite traits that are altered in response to novel within-vector environments (Chapter 4), (iii) how changes to vector biology as a consequence of vector control directly and/or indirectly affect parasite fitness (Chapter 5), and (iv) if parasite transmission potential and fitness can be better estimated (Chapter 6).

My empirical results reveal that there are strain-specific differences in within-vector parasite traits important for transmission (Chapter 3), suggesting that there is underlying genetic variation for natural selection to act upon. In addition, I show that both parasite (Chapter 4) and vector traits (Chapter 5) exhibit plastic strategies in response to variation in the availability of nutritional resources. My findings (Chapter 4) suggest that while parasites are constrained by limited access to nutritional resources, they will actively adjust their within-vector development to best exploit the resources available in ways that maximise transmission. I also demonstrate (Chapter 5) that the timing and propensity of vector biting is dependent on their nutritional state; while parasites produce fewer progeny in starved mosquitoes, these mosquitoes have a higher propensity to bite, and are also more likely to forage at a non-classical biting time when humans are unprotected by bed nets. Finally, I develop and test a non-destructive assay to track parasite development over time (Chapter 6) and demonstrate that while parasites expelled in mosquito saliva during sugar feeding are detectable, increasing the detection rate is required to maximise the utility of these assays for quantifying transmission dynamics.

Together, my results reveal that malaria parasites demonstrate considerable variation in within-vector traits and can plastically respond to changes in their environment in manners that appear adaptive. Thus, my findings suggest that parasites have the ability to evolve and plastically change fitness-determining traits, many of which are affected by vector control tool use. However, my work also demonstrates that within-vector environmental variation (such as resource availability) can influence the transmission potential of parasites and vectors in opposing ways and may have complex consequences for disease dynamics. Therefore, investigating how and why both vector and parasite phenotypes respond to environmental change is necessary for understanding for how natural selection will shape disease transmission and parasite evolution, especially in response to current and future control interventions.