Underexplored diversity of gill monogeneans in cichlids from Lake Tanganyika: eight new species of  Cichlidogyrus  Paperna, 1960 (Monogenea: Dactylogyridae) from the northern basin of the lake, with remarks on the vagina and the heel of the male copulatory organ

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Abstract

Background

Lake Tanganyika harbours the most diverse cichlid assemblage of the Great African Lakes. Considering its cichlid flocks consist of approximately 250 endemic species, we can hypothesize a high species-richness in their often quite host-specific monogenean ectoparasites belonging to Cichlidogyrus Paperna, 1960. Yet, only 24 species were described from Tanganyikan hosts and some host tribes have never been investigated for monogeneans. This study presents the first parasitological examination of species of the tribes Cyprichromini ( Cyprichromis microlepidotus (Poll, 1956)), Eretmodini ( Eretmodus marksmithi Burgess, 2012 and Tanganicodus irsacae Poll, 1950) and Ectodini ( Aulonocranus dewindti (Boulenger, 1899)). Specimens of the ectodine Ophthalmotilapia nasuta (Poll & Matthes, 1962) from which four Cichlidogyrus spp. have been previously described from more southern localities were also studied. Further, we discuss the haptor configuration in Tanganyikan Cichlidogyrus spp. and highlight the morphological diversity of the vagina, and that of the heel, a sclerotized part of the male copulatory organ, absent in some species of Cichlidogyrus.

Methods

Cichlidogyrus spp. were isolated from gills and fixed using GAP. Haptoral and genital hard parts were measured and drawn by means of a phase contrast microscopic examination.

Results

We describe eight new species: Cichlidogyrus milangelnari n. sp. on C. microlepidotus; C. jeanloujustinei n. sp. on E. marksmithi; C. evikae n. sp. on T. irsacae; C. aspiralis n. sp., C. glacicremoratus n. sp. and C. rectangulus n. sp. on O. nasuta; and C. pseudoaspiralis n. sp. and C. discophonum n. sp. on A. dewindti. Three haptoral morphotypes were recognized among the new species. Species of Cichlidogyrus from closely related hosts exhibited the same morphotypes. Geographical variation in Cichlidogyrus spp. fauna as observed in O. nasuta and three morphotypes were distinguished. Finally, we listed 111 Cichlidogyrus species, of which 27 and three Tanganyikan species lack sclerotized vagina and heel, respectively, just like 19 and seven species outside of the lake.

Conclusions

Haptoral and genital features in the Tanganyikan Cichlidogyrus fauna reflect the phylogenetic relationships of their cichlid hosts. It seems that several lineages of Cichlidogyrus spp. exist in Lake Tanganyika but further studies are necessary to confirm this hypothesis and answer questions related to Lake Tanganyika and its cichlids.

Electronic supplementary material

The online version of this article (10.1186/s13071-017-2460-6) contains supplementary material, which is available to authorized users.

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Most cited references 58

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Lake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes.

E Verheyen, L Rüber, C Sturmbauer … (2001)

Water level fluctuations are important modulators of speciation processes in tropical lakes, in that they temporarily form or break down barriers to gene flow among adjacent populations and/or incipient species. Time estimates of the most recent major lowstands of the three African Great Lakes are thus crucial to infer the relative timescales of explosive speciation events in cichlid species flocks. Our approach combines geological evidence with genetic divergence data of cichlid fishes from the three Great East African Lakes derived from the fastest-evolving mtDNA segment. Thereby, we show for each of the three lakes that individuals sampled from several populations which are currently isolated by long geographic distances and/or deep water form clusters of equally closely related haplotypes. The distribution of identical or equally closely related haplotypes in a lake basin allows delineation of the extent of lake level fluctuations. Our data suggest that the same climatic phenomenon synchronized the onset of genetic divergence of lineages in all three species flocks, such that their most recent evolutionary history seems to be linked to the same external modulators of adaptive radiation. A calibration of the molecular clock of the control region was elaborated by gauging the age of the Lake Malawi species flock through the divergence among the utaka-cichlid and the mbuna-cichlid lineages to minimally 570,000 years and maximally 1 Myr. This suggests that the low-lake-level period which established the observed patterns of genetic relatedness dates back less than 57,000 years, probably even to 17,000-12,400 years ago, when Lake Victoria dried up and Lakes Malawi and Tanganyika were also low. A rapid rise of all three lakes about 11,000 years ago established the large-scale population subdivisions observed today. Over that period of time, a multitude of species originated in Lakes Malawi and Victoria with an impressive degree of morphological and ecological differentiation, whereas the Tanganyikan taxa that were exposed to the same habitat changes hardly diverged ecologically and morphologically. Our findings also show that patterns of genetic divergences of stenotopic organisms provide valuable feedback on geological and sedimentological time estimates for lake level changes.

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Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish.

Milan Gelnar, Andrea Šimková, Olivier Verneau … (2006)

Patterns and likely processes connected with evolution of host specificity in congeneric monogeneans parasitizing fish species of the Cyprinidae were investigated. A total of 51 Dactylogyrus species was included. We investigated (1) the link between host specificity and parasite phylogeny; (2) the morphometric correlates of host specificity, parasite body size, and variables of attachment organs important for host specificity; (3) the evolution of morphological adaptation, that is, attachment organ; (4) the determinants of host specificity following the hypothesis of specialization on more predictable resources considering maximal body size, maximal longevity, and abundance as measures of host predictability; and (5) the potential link between host specificity and parasite diversification. Host specificity, expressed as an index of host specificity including phylogenetic and taxonomic relatedness of hosts, was partially associated with parasite phylogeny, but no significant contribution of host phylogeny was found. The mapping of host specificity into the phylogenetic tree suggests that being specialist is not a derived condition for Dactylogyrus species. The different morphometric traits of the attachment apparatus seem to be selected in connection with specialization of specialist parasites and other traits favored as adaptations in generalist parasites. Parasites widespread on several host species reach higher abundance within hosts, which supports the hypothesis of ecological specialization. When separating specialists and generalists, we confirmed the hypothesis of specialization on a predictable resource; that is, specialists with larger anchors tend to live on fish species with larger body size and greater longevity, which could be also interpreted as a mechanism for optimizing morphological adaptation. We demonstrated that ecology of host species could also be recognized as an important determinant of host specificity. The mapping of morphological characters of the attachment organ onto the parasite phylogenetic tree reveals that morphological evolution of the attachment organ is connected with host specificity in the context of fish relatedness, especially at the level of host subfamilies. Finally, we did not find that host specificity leads to parasite diversification in congeneric monogeneans.

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Monogeneans of West African Cichlid Fish: Evolution and Cophylogenetic Interactions

Monika Mendlová, Yves Desdevises, Kristína Civáňová … (2012)

The goals of this paper were to investigate phylogenetic and evolutionary patterns of cichlid fish from West Africa and their Cichlidogyrus and Scutogyrus monogenean parasites, to uncover the presence of host-parasite cospeciation and to assess the level of morphological adaptation in parasites. This required the following steps, each one representing specific objectives of this paper: (1) to build phylogenetic trees for Cichlidogyrus and Scutogyrus species based on ribosomal DNA sequences, (2) to investigate phylogenetic relationships within West African cichlid fish based on the analysis of mitochondrial cytochrome b DNA sequences, (3) to investigate host-parasite cophylogenetic history to gain clues on parasite speciation process, and (4) to investigate the link between the morphology of the attachment apparatus and parasite phylogeny. Phylogenetic analyses supported the monophyletic origin of the Cichlidogyrus/Scutogyrus group, and suggested that Cichlidogyrus is polyphyletic and that Scutogyrus is monophyletic. The phylogeny of Cichlidae supported the separation of mouthbrooders and substrate-brooders and is consistent with the hypothesis that the mouthbrooding behavior of Oreochromis and Sarotherodon evolved from substrate-brooding behavior. The mapping of morphological characters of the haptor onto the parasite phylogenetic tree suggests that the attachment organ has evolved from a very simple form to a more complex one. The cophylogenetic analyses indicated a significant fit between trees using distance-based tests, but no significant cospeciation signal using tree-based tests, suggesting the presence of parasite duplications and host switches on related host species. This shed some light on the diversification process of Cichlidogyrus species parasitizing West African cichlids.

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Author and article information

Contributors

Chahrazed Rahmouni: rahmouni.chahrazed@gmail.com

Maarten P. M. Vanhove: maarten.vanhove@kuleuven.be

Andrea Šimková: simkova@sci.muni.cz

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 2 December 2017

Publication date PMC-release: 2 December 2017

Publication date Collection: 2017

Volume: 10

Electronic Location Identifier: 591

Affiliations

[1 ]ISNI 0000 0001 2194 0956, GRID grid.10267.32, Department of Botany and Zoology, Faculty of Science, , Masaryk University, ; Kotlářská 2, CZ-611 37 Brno, Czech Republic

[2 ]ISNI 0000 0001 2171 9581, GRID grid.20478.39, Capacities for Biodiversity and Sustainable Development (CEBioS), Operational Directorate Natural Environment, , Royal Belgian Institute of Natural Sciences, ; Vautierstraat 29, B-1000 Brussels, Belgium

[3 ]ISNI 0000 0001 0668 7884, GRID grid.5596.f, Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, , University of Leuven, ; Charles Deberiotstraat 32, B-3000 Leuven, Belgium

[4 ]ISNI 0000 0001 0604 5662, GRID grid.12155.32, Centre for Environmental Sciences, Research Group Zoology: Biodiversity & Toxicology, , Hasselt University, ; Agoralaan Gebouw D, B-3590 Diepenbeek, Belgium

Article

Publisher ID: 2460

DOI: 10.1186/s13071-017-2460-6

PMC ID: 5712084

PubMed ID: 29197419

SO-VID: f8b92d95-7690-4565-a0f3-d3ee74718d35

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 16 November 2016

Date accepted : 9 October 2017

Funding

Funded by: Czech Science Foundation

Award ID: P505/12/G112

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: africa,burundi,cichlidae,cyprichromini,ectodini,eretmodini,platyhelminthes,monogenea,cichlidogyrus

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ScienceOpen disciplines: Parasitology

Keywords: africa, burundi, cichlidae, cyprichromini, ectodini, eretmodini, platyhelminthes, monogenea, cichlidogyrus

Underexplored diversity of gill monogeneans in cichlids from Lake Tanganyika: eight new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) from the northern basin of the lake, with remarks on the vagina and the heel of the male copulatory organ

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Conclusions

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Most cited references 58

Lake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes.

Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish.

Monogeneans of West African Cichlid Fish: Evolution and Cophylogenetic Interactions

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