Monitoring and predicting snail-borne diseases: a multidisciplinary approach

Human activities have become the principal drivers of global change, encompassing habitat destruction and fragmentation, land use change, pollution, overexploitation, and climate change. These processes exert profound influences on terrestrial and aquatic ecosystems, with climate change, in particular, altering freshwater ecosystems through rising temperatures, increased evaporation, reduced oxygen levels, shifting precipitation patterns, and heightened occurrences of extreme events such as heatwaves and droughts. Such changes significantly impact the species inhabiting these aquatic environments, including disease vectors.

Schistosomiasis, a tropical parasitic disease afflicting more than 200 million individuals worldwide, is transmitted through freshwater snails. However, the response of these snails to climate change and the influence on the transmission dynamics of the disease remain uncertain. Species can navigate climate change by adapting to changing environmental conditions or by dispersing to more suitable habitats. The extent to which each of these strategies applies to intermediate host snails of schistosomiasis remains uncertain. This PhD thesis investigates the local adaptation potential of the schistosome intermediate snail host, Bulinus truncatus, to temperature, and assesses how climate change will affect the distribution of this species.

The thesis commences by conducting an extensive review of the literature on the ecology of African intermediate snail hosts of schistosomiasis. This systematic review identifies temperature and precipitation as key drivers of large-scale snail distributions, with water chemistry and waterbody characteristics determining snail distributions at a regional level. However, it also reveals a fragmented body of research spanning several decades, characterized by significant knowledge gaps and limited, often flawed, studies with small sample sizes, pseudoreplication, or insufficient replicates. As a result, the dataset is deemed unreliable for assessing the impact of climate change on these intermediate host snails.

Given the pivotal role of temperature in shaping snail distributions, the thesis explores the effects of temperature on the life-history traits of B. truncatus. As the intermediate snail host with the broadest distribution, B. truncatus plays a crucial role in determining the maximum geographical extent of schistosomiasis, making it an ideal subject to explore the impact of climate change on the distribution of the disease. The findings reveal that B. truncatus demonstrates substantial local adaptation in terms of phenology, physiology, and genetic makeup. Adaptations of life-history traits are evident, with warm-origin snails characterised by reduced growth and survival rates at higher temperatures that are compensated by higher reproduction rates. In contrast, cold-origin snails exhibit higher growth rates, optimizing their performance in shorter growing seasons. Physiological adaptations include elevated sugar and haemoglobin content in cold-adapted snails, enhancing mobility at lower temperatures. Warm-adapted snails exhibit increased protein levels that might be attributed to increased levels of heat-shock proteins, protecting their proteins from denaturation under high temperatures, but they also show greater oxidative damage, which could limit their lifespan. Additionally, heightened phenoloxidase levels indicate a more robust immune response to parasites in snails from regions with higher parasite diversity. Moreover, an analysis of single nucleotide polymorphisms identifies 633 outlier markers associated with temperature or precipitation, putatively providing a genetic basis for these adaptations and underscoring the species' high potential to adapt to changing climate conditions.

Subsequently, the thesis models the present and future distribution of B. truncatus by integrating both correlative and mechanistic species distribution models. While correlative models correlate species observations with environmental variables, mechanistic models incorporate explicit ecological knowledge to build process-explicit models. The combined approach predicts an up to 33 % increase in the area suitable habitat for B. truncatus by 2080-2100, predominantly in Central Africa and Southern Europe, while habitat suitability declines in the Sahel region. The current habitat suitability predictions closely align with areas of high schistosomiasis prevalence, suggesting that these models can be employed for schistosomiasis risk assessment. This implies a potential decrease in schistosomiasis risk in the Sahel, a highly endemic region, and an increase in risk in Southern Europe and Central Africa.

While the results of this thesis do not directly enable local distribution forecasts, they serve to identify broader regions where schistosomiasis prevalence may change. Consequently, monitoring programs can be implemented to track potential snail or parasite invasions, and early control measures can be employed to mitigate the risk of new disease outbreaks. Furthermore, acquiring additional data on the ecology of intermediate hosts and developing microclimatic models for freshwater habitats can enhance regional-scale snail distribution models. Additionally, the high capacity for local adaptation of the snails suggests that they may adapt to other factors, such as parasitism, predation, or pesticides which could have implications for the emergence of schistosomiasis in new areas and the efficiency of snail control measures. Especially in regions where molluscicides are regularly applied or natural predators are present, high levels of local adaptation could potentially lead to molluscicide resistance or predator evasion behaviour.

In conclusion, this thesis advances our understanding of the response of schistosome intermediate snail hosts to temperature and their potential for local adaptation. Additionally, it sheds light on how climate change may influence the distribution of these hosts and, consequently, the dynamics of schistosomiasis transmission.