Dataset Information

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.

SUBMITTER: Vanhove MP

PROVIDER: S-EPMC4558575 | biostudies-literature | 2015 Sep

REPOSITORIES: biostudies-literature

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

Vanhove Maarten P M MP Pariselle Antoine A Van Steenberge Maarten M Raeymaekers Joost A M JA Hablützel Pascal I PI Gillardin Céline C Hellemans Bart B Breman Floris C FC Koblmüller Stephan S Sturmbauer Christian C Snoeks Jos J Volckaert Filip A M FA Huyse Tine T

Scientific reports 20150903

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 s ...[more]

PMID: 26335652

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Project description:BackgroundThe tribe Lamprologini is the major substrate breeding lineage of Lake Tanganyika's cichlid species flock. Among several different life history strategies found in lamprologines, the adaptation to live and breed in empty gastropod shells is probably the most peculiar. Although shell-breeding arose several times in the evolutionary history of the lamprologines, all obligatory and most facultative shell-breeders belong to the so called "ossified group", a monophyletic lineage within the lamprologine cichlids. Since their distinctive life style enables these species to live and breed in closest vicinity, we hypothesized that these cichlids might be particularly prone to accidental hybridization, and that introgression might have affected the evolutionary history of this cichlid lineage.ResultsOur analyses revealed discrepancies between phylogenetic hypotheses based on mitochondrial and nuclear (AFLP) data. While the nuclear phylogeny was congruent with morphological, behavioral and ecological characteristics, several species--usually highly specialized shell-breeders--were placed at contradicting positions in the mitochondrial phylogeny. The discordant phylogenies strongly suggest repeated incidents of introgressive hybridization between several distantly related shell-breeding species, which reticulated the phylogeny of this group of cichlids. Long interior branches and high bootstrap support for many interior nodes in the mitochondrial phylogeny argue against a major effect of ancient incomplete lineage sorting on the phylogenetic reconstruction. Moreover, we provide morphological and genetic (mtDNA and microsatellites) evidence for ongoing hybridization among distantly related shell-breeders. In these cases, the territorial males of the inferred paternal species are too large to enter the shells of their mate, such that they have to release their sperm over the entrance of the shell to fertilize the eggs. With sperm dispersal by water currents and wave action, trans-specific fertilization of clutches in neighboring shells seem inevitable, when post-zygotic isolation is incomplete.ConclusionFrom the direct observation of hybrids we conclude that hybridization between distantly related gastropod-shell-breeding cichlids of Lake Tanganyika follows inevitably from their ecological specialization. Moreover, the observed incongruence between mtDNA and nuclear multilocus phylogeny suggests that repeated hybridization events among quite distantly related taxa affected the diversification of this group, and introduced reticulation into their phylogeny.

Project description:The unparalleled biodiversity of Lake Tanganyika (Africa) has fascinated biologists for over a century; its unique cichlid communities are a preferred model for evolutionary research. Although species delineation is, in most cases, relatively straightforward, higher-order classifications were shown not to agree with monophyletic groups. Here, traditional morphological methods meet their limitations. A typical example are the tropheine cichlids currently belonging to Simochromis and Pseudosimochromis. The affiliations of these widespread and abundant cichlids are poorly understood. Molecular work suggested that genus and species boundaries should be revised. Moreover, previous morphological results indicated that intraspecific variation should be considered to delineate species in Lake Tanganyika cichlids. We review the genera Simochromis and Pseudosimochromis using an integrative approach. Besides a morphometric study and a barcoding approach, monogenean Cichlidogyrus (Platyhelminthes: Ancyrocephalidae) gill parasites, often highly species-specific, are used as complementary markers. Six new species are described. Cichlidogyrus raeymaekersi sp. nov., C. muterezii sp. nov. and C. banyankimbonai sp. nov. infect S. diagramma. Cichlidogyrus georgesmertensi sp. nov. was found on S. babaulti and S. pleurospilus, C. franswittei sp. nov. on both S. marginatus and P. curvifrons and C. frankwillemsi sp. nov. only on P. curvifrons. As relatedness between Cichlidogyrus species usually reflects relatedness between hosts, we considered Simochromis monotypic because the three Cichlidogyrus species found on S. diagramma belonged to a different morphotype than those found on the other Simochromis. The transfer of S. babaulti, S. marginatus, S. pleurospilus and S. margaretae to Pseudosimochromis was justified by the similarity of their Cichlidogyrus fauna and the intermediate morphology of S. margaretae. Finally parasite data also supported the synonymy between S. pleurospilus and S. babaulti, a species that contains a large amount of geographical morphological variation.

Project description:A long history of research focused on the East Africa cichlid radiations (EAR) revealed discrepancies between mtDNA and nuclear phylogenies, suggesting that interspecific hybridisation may have been significant during the radiation of these fishes. The approximately 250 cichlid species of Lake Tanganyika have their roots in a monophyletic African cichlid assemblage, but controversies remain about the precise phylogenetic origin and placement of different lineages and consequently about L. Tanganyika colonization scenarios. 3312 AFLP loci and the mitochondrial ND2 gene were genotyped for 91 species representing almost all major lacustrine and riverine haplotilapiine east African cichlid lineages with a focus on L. Tanganyika endemics. Explicitly testing for the possibility of ancient hybridisation events, a comprehensive phylogenetic network hypothesis is proposed for the origin and diversification of L. Tanganyika cichlids. Inference of discordant phylogenetic signal strongly suggests that the genomes of two endemic L. Tanganyika tribes, Eretmodini and Tropheini, are composed of an ancient mixture of riverine and lacustrine lineages. For the first time a strong monophyly signal of all non-haplochromine mouthbrooding species endemic to L. Tanganyika ("ancient mouthbrooders") was detected. Further, in the genomes of early diverging L. Tanganyika endemics Trematocarini, Bathybatini, Hemibatini and Boulengerochromis genetic components of other lineages belonging to the East African Radiation appear to be present. In combination with recent palaeo-geological results showing that tectonic activity in the L. Tanganyika region resulted in highly dynamic and heterogeneous landscape evolution over the Neogene and Pleistocene, the novel phylogenetic data render a single lacustrine basin as the geographical cradle of the endemic L. Tanganyika cichlid lineages unlikely. Instead a scenario of a pre-rift origin of several independent L. Tanganyika precursor lineages which diversified in ancient rivers and precursor lakes and then amalgamated in the extant L. Tanganyika basin is put forward as an alternative: the 'melting pot Tanganyika' hypothesis.

Dataset Information

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

Publications

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

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