Contrasting Host-Parasite Population Structure: Morphology and Mitogenomics of a Parasitic Flatworm on Pelagic Deepwater Cichlid Fishes from Lake Tanganyika

SIMPLE SUMMARY: Species richness in open water areas is generally lower than in coastal zones. Fish parasites have been targeted as biological tags potentially magnifying biological patterns of their hosts including long-distance migrations notoriously difficult to trace. Lake Tanganyika (Africa) is an ideal place to study general mechanisms of host-parasite interactions in an open water environment and Cichlidogyrus, a monogenean flatworm lineage also present in Lake Tanganyika, has been proposed as a model system to study parasite-host relationships. The present study revealed the lake-wide occurrence (600 km) of Cichlidogyrus casuarinus, a parasite with a broad host range infecting pelagic fishes endemic to Lake Tanganyika. Our comparative approach highlighted incongruence between morphological and genetic differentiation of the populations of Cichlidogyrus casuarinus. Our results show a limitation of the parasite’s magnifying potential for the focal host species due to the parasites’ broad host range including highly mobile host species. Using different sequencing technologies, the study further provides the first assessment of the genetic variation of mitochondrial data in Cichlidogyrus showing contrasting patterns within and between parasite species. Given the now considerable baseline knowledge on its morphological and genetic variation, we propose C. casuarinus as a model to study (1) mechanisms driving host range and (2) the role of phenotypic plasticity in diversification and speciation. ABSTRACT: Little phylogeographic structure is presumed for highly mobile species in pelagic zones. Lake Tanganyika is a unique ecosystem with a speciose and largely endemic fauna famous for its remarkable evolutionary history. In bathybatine cichlid fishes, the pattern of lake-wide population differentiation differs among species. We assessed the congruence between the phylogeographic structure of bathybatine cichlids and their parasitic flatworm Cichlidogyrus casuarinus to test the magnifying glass hypothesis. Additionally, we evaluated the use of a PoolSeq approach to study intraspecific variation in dactylogyrid monogeneans. The lake-wide population structure of C. casuarinus ex Hemibates stenosoma was assessed based on a portion of the cox1 gene combined with morphological characterisation. Additionally, intraspecific mitogenomic variation among 80 parasite samples from one spatially constrained metapopulation was assessed using shotgun NGS. While no clear geographic genetic structure was detected in parasites, both geographic and host-related phenotypic variation was apparent. The incongruence with the genetic north-south gradient observed in H. stenosoma may be explained by the broad host range of this flatworm including eupelagic bathybatine host species that form panmictic populations across the lake. In addition, we present the first parasite mitogenome from Lake Tanganyika and propose a methodological framework for studying the intraspecific mitogenomic variation of dactylogyrid monogeneans.