A flatworm’s choice: developing a model system to study the ecology and evolution of host preference using cichlid fishes and their monogenean parasites

Abstract

Understanding the underlying principles of host selection is becoming of increasing importance in a world where human impact increases the risk of emerging infectious diseases. What enables and drives a parasite species to expand its host range? Model systems of parasite eco-evolutionary processes might help us address this question. Yet most parasites models include only few host species with a strong bias towards human parasites, or many distantly related host or parasite lineages, with evolutionary processes that lie too far in the past. Here, we present the cichlid-Cichlidogyrus system consisting of 137 parasitic flatworms (Monogenea: Dactylogyridae) and 144 host species (Cichlidae) across Africa (in 2019), both forming well-defined monophyletic taxa. In a four-year period, we investigated eco-evolutionary processes using molecular, morphological, infection, and host ecological data through literature surveys, network analyses, phylogenetics, whole-genome sequencing, machine learning, and quantitative PCR. This dissertation consists of two major parts (following the introduction in Chapter 1). Part 1 (Chapter 2–4) establishes a baseline using the data of 10,529 infected hosts reported from the literature, 223 DNA sequences from four different DNA regions and 58 parasite species, and morphometrics of 1869 parasite specimens. Highlights of our results included: (2) an updated phylogenetic analysis with a 57% increase in coverage of described species (to 40% of all described species) , (2, 3) an overview of the phylogenetic informativeness of morphological characters at the genus and family level, (2) the detection of an evolutionary rate shift of the parasites infecting an adaptive host radiation reflected by the attachment organ morphology, and (4) the identification of the host phylogeny and ecology as main determinants of host repertoires. Part 2 (Chapter 5–7) explores phenotypic aspects highlighted in Part 1 empirically in more detail by investigating the monogenean biodiversity in a hitherto neglected lineage of hosts (Chromidotilapiini), the functional biology of species of Cichlidogyrus, especially genes involved in stress response pathways, and the viability of real-time quantitative PCR to quantify ratios of mitochondrial (mtDNA) and nuclear DNA (ncDNA) content. We described nine new species of monogeneans (5). Furthermore, we detected several cases of expansions and losses of families of stress response genes (6), and we summarised challenges and potential alternative for mtDNA quantification (7). In the course of this project, we expanded morphological, evolutionary, and ecological outcome measures and addressed knowledge gaps and biases in West and Central Africa. These results and data as well as the broad scope in terms of methodologies makes the cichlid-Cichlidogyrus system the first species-rich host-parasite system to be investigated to this extent. However, with a majority of species still undescribed, a majority of described species unsequenced, and research on monogenean functional biology only its infancy, the system still has to realise its full potential.