Evolution of parasite reproductive strategies in natural infections

Predicting how parasites adapt to their environment is becoming increasingly important. For example, changes to: the climate, composition of host-parasite-vector communities, and habitat, are implicated in the emergence of new infectious diseases of wildlife, crop species, livestock, and humans. More broadly, the in-host environment experienced by parasites also varies rapidly and extensively. Understanding how parasites cope with a variable in-host environment is central to understanding disease and infectiousness, as well as providing a framework for predicting parasite evolution in response to other changes in their ecology. We will use evolutionary theory to ask fundamental questions in evolutionary biology and infectious disease research: how do reproductive (transmission) strategies of protozoan parasites evolve? This group includes malaria (Plasmodium) parasites and cause some of the most serious pathogens of livestock, companion animals, wildlife, and humans. Despite the economic, medical, and veterinary importance of understanding the transmission strategies of malaria parasites, over a century of research has yielded remarkably little understanding of their basic reproductive biology. However, rapid progress has been made in recent years: new molecular tools have been developed and applied in an evolutionary framework to ask questions about parasite transmission. Data from this new approach are overturning the conventional wisdom: from the epidemiology of parasites to their behaviour during infections. For example, we have discovered that parasites fine-tune the production and sex ratio of transmission stages in remarkably sophisticated ways; according to their density within hosts, competition with other parasite strains, and whether their hosts are anaemic, mounting an immune response, or receiving drug treatment. These 'plastic family planning strategies' enable parasites to maximise transmission by matching their behaviour to the changing conditions they face during infections. However, these studies have focused on model parasites in laboratory experiments - whether these 'sophisticated' strategies occur in natural infections is controversial. We will address this by developing sensitive methods to quantify the production and sex ratio of transmission (reproductive) stages of human malaria (P. falciparum) parasites in the wild and testing whether evolutionary theory can explain their strategies. We have already developed these methods for a related species of malaria parasite and laid the groundwork for translating this assay to human parasites. Evolutionary theory predicts that parasite reproductive strategies will be shaped by the variation in their in-host environment that they encounter during infections. Most studies on parasite transmission have focused on either the number or sex ratio of transmission stages but evolutionary theory predicts these traits are simultaneously optimised - therefore they need to be investigated together and can only be understood in the context of each other. Explaining variation in the life-history traits exhibited by individuals is a major aim in evolutionary biology. There is also increasing interest in using an evolutionary approach to understand how parasite life-history traits shape within-infection dynamics and contribute to virulence and transmission. Given the sophisticated parasite strategies recently observed in lab experiments, investigating the behaviour of parasites in natural infections is timely and important. Understanding plasticity in the reproductive strategies of parasites is also central to predicting their short- and long-term responses to changes in their ecology: such as how habitat change, host shifts, or control measures influence the spread of disease.