Patterns and processes of diversification in African pulmonate gastropods of zoonotic, biomedical and veterinary importance

Abstract

Vector-borne tropical diseases cause significant impacts on the ecological, economic, and social aspects of society. It is estimated that hundreds of millions of people, particularly in sub-Saharan Africa, are affected directly or indirectly by these diseases. Freshwater gastropods play an important role as intermediate hosts (IHs) for the causative agents of parasitic diseases such as schistosomiasis (bilharzia) and fascioliasis. While many aspects of the diseases can be considered relatively well studied, comparatively little is known about the biology, ecology, and eco-evolutionary dynamics of the intermediate hosts. A shift in the prevalence distribution threshold of schistosomiasis to higher altitudes above 1,600 m in crater lakes of western Uganda, moreover assumed to be linked to climate change, raised concerns. It is precisely the dynamics of the intermediate hosts that determine the disease prevalence and so focusing on these is regarded as the most promising control strategy for the declared goal of the complete elimination of schistosomiasis and fascioliasis. Especially with regard to climate change, dramatic shifts in the occurrence of intermediate hosts with important consequences for tropical diseases are predicted. The present dissertation, therefore, addresses aspects of evolutionary biology such as speciation patterns and processes, phylogenetic and biogeographical relationships, and dynamics of selected intermediate hosts of different genera. In particular, historical but also recent ecological factors that are taken into account have led to the current occurrence patterns and thus to the occurrence or non-occurrence of parasites and diseases. Various case studies, primarily on the genus Bulinus, but also on Biomphalaria and Galba, were carried out on a regional and continental scale. The sampling area covers various landscapes and altitudinal ranges, and a variety of geological and ecological aspects. The snail intermediate hosts of human and veterinary importance for dozens of crater lakes in western Uganda were molecularly identified and phylogenetically investigated. The interplay between biotic and abiotic elements that regulate the presence of intermediate hosts was analysed. In this system, Biomphalaria snails the intermediate hosts for the Schistosoma mansoni that causes the intestinal form of schistosomiasis dominate, while Bulinus snails though equally dominant, are mostly of a species (Bulinus tropicus) that hosts Schistosoma bovis parasites that affect livestock. A high level of diversification was realized in these small and relatively young crater lakes. The small-scale analysis of the biotic and abiotic factors revealed that the intermediate hosts Biomphalaria and Bulinus require simply a suitable freshwater habitat just like other gastropods. The colonization of these East African rift valley freshwater systems is attributed to the surrounding great lakes system. The study was expanded to include the Lake Victoria system, which has been noted as one of the significant biodiversity source reservoirs for the crater lakes. Despite being quite vast and having a variety of ecological niches characterized by shallow and ecologically suited shorelines and banks of the main waterbody and islands, Lake Victoria displays an array of Bulinus populations that is less diverse. Generally, there is more species diversity and genetic diversity in the genus Bulinus and therefore the potential for urogenital schistosomiasis is much higher than previously known. Two studies on a continental scale were carried out for the genera Bulinus and Galba with a special focus on Afromontane regions, as these will play an important role in the future occurrence of tropical diseases in the course of the predicted climate change. Multigene phylogenies were recronstructed for both genera based on an Africa-wide data set. A previously unknown cryptic species was found for the genus Galba, which acts as an intermediate host for the liver fluke (Fasciola hepatica) throughout sub-Saharan Africa. For both genera, the various mountain regions were already settled several times in the Plio-Pleistocene. Though the high altitude colonization for species B. truncatus/tropicus complex is comparatively more recent, they have more extensively evolved in higher altitudes than the other Bulinus species groups. As a result, the study defines a new high altitude distribution threshold of ~4000 m above sea level. Several unknown lineages and species, particularly at extreme altitudes on Mt. Elgon/Uganda and in Lesotho, have been identified. The multimarker phylogenetic analysis also helped to finally resolve the disputed relationship between the four Bulinus species groups. All work in this dissertation contributes to a better understanding of the biodiversity and evolution of intermediate hosts. They thus represent an important basis for scenarios for the future development of occurrence and prevalence as well as more successful strategies to combat the neglected but extremely important tropical diseases schistosomiasis and fasciolosis.