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

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.

Host lifestyle and parasite interspecific facilitation mediate co-infection in a species-poor host-parasite system

“…Habitat differences between the clupeid hosts over their lifespan most likely drive contrasting spatial patterns of infection between closely related parasite species. This result further supports the importance of host species with the highest dispersal capacity on the spatial distribution of parasites, as reported for Cichlidogyrus casuarinus Pariselle, Muterezi Bukinga & Vanhove, 2015 infecting pelagic cichlids in the lake (Kmentová et al, 2021). Contrasting levels of gene flow between the two parasite species related to geographic origin along the North-South axis of the lake (Kmentová et al, Under review) may therefore be associated with lifestyle differences between the two clupeid species.…”

“…Habitat differences between the clupeid hosts over their lifespan most likely drive contrasting spatial patterns of infection between closely related parasite species. This result further supports the importance of host species with the highest dispersal capacity on the spatial (Kmentová et al, 2021).…”

Ectoparasitism in Polystomatidae (Neodermata, Monogenea): phylogenetic position and mitogenome of Sphyranura euryceae, a parasite of the Oklahoma salamander

“…Comparison with the mitochondrial genome of D. hangzhouensis reveals similar gene order, with two instances of rearrangement in the order of adjacent tRNA genes between the two species. However, the order of protein coding genes was conserved between the two species as has been observed in other monogenean families such as Dactylogyridae [45,46]. However, we identify differences in start/stop codon usage in 8 of 12 protein coding genes between the two polystomatids.…”

Somewhere I belong: phylogeny and morphological evolution in a species‐rich lineage of ectoparasitic flatworms infecting cichlid fishes

“…1c) and host range data for 136 species belonging to Cichlidogyrus. Raw measurements taken through light microscopy were assembled from AP's personal morphometric database and from the raw data of previous publications (Geraerts et al, 2020;Gillardin et al, 2012;Gobbin et al, 2021;Igeh et al, 2017;Kmentov a et al, 2016aKmentov a et al, , 2016bKmentov a et al, , 2016cMessu Mandeng et al, 2015;Muterezi Bukinga et al, 2012;Pariselle et al, 2013;Pariselle and Euzet, 2003;Rahmouni et al, 2017Rahmouni et al, , 2018Rehulkov a et al, 2013;Vanhove et al, 2011). Raw measurements were deposited at MorphoBank (www.…”

“…Species of Cichlidogyrus rival (Cruz‐Laufer et al., 2021) and possibly exceed (see Poulin, 2014) their hosts in terms of species numbers: 137 parasite species have been described on 126 fish species (Cruz‐Laufer et al., 2021). Monogenean flatworms have provided insight into parasite speciation (Meinilä et al., 2004; Šimková et al., 2013; Vanhove et al., 2015), population dynamics (Kmentová et al., 2021), anthropogenic introductions (Jorissen et al., 2020; Šimková et al., 2019) and host biogeography (Barson et al., 2010; Pariselle et al., 2011; Vanhove et al., 2013, 2016). These gill parasites are well‐shielded from external physical forces by the gill flaps and are, therefore, found on many specimens in historical museum collections as by‐products of host samplings (Jorissen et al., 2020).…”