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.

Reduced host-specificity in a parasite infecting non-littoral Lake Tanganyika cichlids evidenced by intraspecific morphological and genetic diversity

“…The previously proposed low host-specificity of C. casuarinus in the deepwater habitat15, which contrasts with the high host-specificity of many of its congeners in the littoral zone8, was supported by the fact that no variation was observed at the three rDNA regions in C. casuarinus sampled across different host species. Nuclear rDNA regions are considered to be suitable markers for species-level identification of monogeneans5962.…”

“…generated by next-generation sequencing approaches) might reveal some population structure8586. However, even if that was the case, it would indicate recent population splitting postdating the ancient divergence of the hosts, since the markers available for this study are generally used to distinguish closely related monogenean populations or species8,55.…”

“…Among monogeneans, a substitution rate estimate for COI is only available for Gyrodactylus (13.7–20.0% per million years;109). In view of the short generation time of Gyrodactylus compared to many other monogeneans110, it can be assumed that mutation rates of other monogeneans are somewhat lower111, and that the employed 10% per million years represents a reasonable approximation8. Two independent MCMC runs of 10 million generations each at a sampling frequency of 1,000 were conducted, with a burn-in of the first 10% of sampled generations.…”

“…It is known for its remarkable species diversity characterised by rapid radiation processes in many vertebrate and invertebrate taxa7, including parasitic flatworms that infect cichlids8. Therefore, it has been intensively studied for many decades.…”

“…This genus displays variation in host-specificity and contains generalist but also strictly specialist species3943. In Lake Tanganyika, most species of Cichlidogyrus described to date are strict or intermediate specialists810121315 following the terminology used in Mendlová & Šimková43. While strict specialists infect only a single host species, intermediate specialists parasitise on two or more congeneric host species and intermediate generalist infect heterogeneric host species from the same tribe.…”