Hidden biodiversity in an ancient lake: phylogenetic congruence between Lake Tanganyika tropheine cichlids and their monogenean flatworm parasites

Abstract

The stunning diversity of cichlid fishes has greatly enhanced our understanding of speciation and radiation. Little is known about the evolution of cichlid parasites. Parasites are abundant components of biodiversity, whose diversity typically exceeds that of their hosts. In the first comprehensive phylogenetic parasitological analysis of a vertebrate radiation, we study monogenean parasites infecting tropheine cichlids from Lake Tanganyika. Monogeneans are flatworms usually infecting the body surface and gills of fishes. In contrast to many other parasites, they depend only on a single host species to complete their lifecycle. Our spatially comprehensive combined nuclear-mitochondrial DNA dataset of the parasites covering almost all tropheine host species (N = 18), reveals species-rich parasite assemblages and shows consistent host-specificity. Statistical comparisons of host and parasite phylogenies based on distance and topology-based tests demonstrate significant congruence and suggest that host-switching is rare. Molecular rate evaluation indicates that species of Cichlidogyrus probably diverged synchronically with the initial radiation of the tropheines. They further diversified through within-host speciation into an overlooked species radiation. The unique life history and specialisation of certain parasite groups has profound evolutionary consequences. Hence, evolutionary parasitology adds a new dimension to the study of biodiversity hotspots like Lake Tanganyika.

Figure 1. Consensus cladogram of flatworms belonging to the genus Cichlidogyrus infecting Lake Tanganyika cichlids.

Cladogram based on the combined nuclear ITS-1, 5.8S rDNA, ITS-2 and mitochondrial COI sequences of Cichlidogyrus parasitizing Lake Tanganyika tropheine cichlids and the outgroups mentioned in Table 2. Statistical support is shown as posterior probability under BI/ML bootstrap. Clades that neither yield a support value of 85 nor of 70 under BI or ML, respectively, were collapsed; “–” indicates that a clade was not recovered in a particular analysis. Tip labels indicate host species with sampling locality and country (C: Democratic Republic of Congo; B: Burundi; T: Tanzania and Z: Zambia) and are coloured according to host genus consistent with Fig. 4. Monophyletic assemblages infecting one host species are boxed. Inlet: Cichlidogyrus parasites (300–400 μm in length) on the gills of Sarotherodon melanotheron Rüppell, 1852 (photograph taken by author A.P.).

Figure 2. Lineages-through-time plot for Cichlidogyrus parasites of Tropheini.

Lineages-through-time plot based on an ultrametric Bayesian ITS rDNA tree, constructed under a relaxed clock model, of Cichlidogyrus living on tropheine hosts; x-axis: time; y-axis: number of lineages (logarithmic scale).

Figure 3. Co-phylogenetic reconciliations of Cichlidogyrus and Tropheini trees.

CoRe-Pa reconciliations of Tropheini (based on AFLP as published by Koblmüller et al.8) and Cichlidogyrus (based on the concatenated nuclear-mitochondrial dataset) trees. Left: second best reconciliation based on a fully resolved parasite ML tree; right: best reconciliation based on a parasite ML tree where nodes with bootstrap support under 70 were collapsed. Branches and tips represent hosts (dark gray) or parasites (dashed/light gray). Drawings made by author T.H.; photographs taken by authors P.I.H. (I. loocki, L. labiatus, Pe. famula, T. moorii), M.P.M.V. (Ps. curvifrons) and M.V.S. (L. dardennii) and reproduced with kind permission from Radim Blažek (‘C.’ horei, ‘G.’ pfefferi, northern Ps. babaulti, S. diagramma, T. duboisi) and Ad Konings (A. burtoni, Pe. fasciolatus, Pe. macrognathus, Pe. polyodon, Pe. trewavasae ephippium, Ps. marginatus, southern Ps. babaulti, T. brichardi).

Figure 4. Lake Tanganyika localities sampled for monogenean cichlid parasites belonging to Cichlidogyrus.

Colour codes refer to the respective host genera; the bottom right map details the sampling localities and major cities. For details, see Table 2. Photographs were taken by authors P.I.H. (I. loocki, L. labiatus, Pe. famula, T. moorii), M.P.M.V. (Ps. curvifrons) and M.V.S. (L. dardennii) and reproduced with kind permission from Radim Blažek (‘C.’ horei, ‘G.’ pfefferi, S. diagramma). Map created using ArcMap v.10 and reproduced with kind permission by Tobias Musschoot.