The first next-generation sequencing approach to the mitochondrial phylogeny of African monogenean parasites (Platyhelminthes: Gyrodactylidae and Dactylogyridae)

Abstract Background Monogenean flatworms are the main ectoparasites of fishes. Representatives of the species-rich families Gyrodactylidae and Dactylogyridae, especially those infecting cichlid fishes and clariid catfishes, are important parasites in African aquaculture, even more so due to the massive anthropogenic translocation of their hosts worldwide. Several questions on their evolution, such as the phylogenetic position of Macrogyrodactylus and the highly speciose Gyrodactylus, remain unresolved with available molecular markers. Also, diagnostics and population-level research would benefit from the development of higher-resolution genetic markers. We aim to offer genetic resources for work on African monogeneans by providing mitogenomic data of four species (two belonging to Gyrodactylidae, two to Dactylogyridae), and analysing their gene sequences and gene order from a phylogenetic perspective. Results Using Illumina technology, the first four mitochondrial genomes of African monogeneans were assembled and annotated for the cichlid parasites Gyrodactylus nyanzae, Cichlidogyrus halli, Cichlidogyrus mbirizei (near-complete mitogenome) and the catfish parasite Macrogyrodactylus karibae (near-complete mitogenome). Complete nuclear ribosomal operons were also retrieved, as molecular vouchers. The start codon TTG is new for Gyrodactylus and for Dactylogyridae, as is the incomplete stop codon TA for Dactylogyridae. Especially the nad2 gene is promising for primer development. Gene order was identical for protein-coding genes and differed between the African representatives of these families only in a tRNA gene transposition. A mitochondrial phylogeny based on an alignment of nearly 12,500 bp including 12 protein-coding and two ribosomal RNA genes confirms that the Neotropical oviparous Aglaiogyrodactylus forficulatus takes a sister group position with respect to the other gyrodactylids, instead of the supposedly ‘primitive’ African Macrogyrodactylus. Inclusion of the African Gyrodactylus nyanzae confirms the paraphyly of Gyrodactylus. The position of the African dactylogyrid Cichlidogyrus is unresolved, although gene order suggests it is closely related to marine ancyrocephalines. Conclusions The amount of mitogenomic data available for gyrodactylids and dactylogyrids is increased by roughly one-third. Our study underscores the potential of mitochondrial genes and gene order in flatworm phylogenetics, and of next-generation sequencing for marker development for these non-model helminths for which few primers are available

Only true pelagics mix : comparative phylogeography of deepwater bathybatine cichlids from Lake Tanganyika

In the absence of dispersal barriers, species with great dispersal ability are expected to show little, if at all, phylogeographic structure. The East African Great Lakes and their diverse fish faunas provide opportunities to test this hypothesis in pelagic fishes, which are presumed to be highly mobile and unrestricted in their movement by physical barriers. Here, we address the link between panmixis and pelagic habitat use by comparing the phylogeographic structure among four deepwater cichlid species of the tribe Bathybatini from Lake Tanganyika. We show that the mitochondrial genealogies (based on the most variable part or the control region) of the four species are very shallow (0.8–4% intraspecific divergence across entire distribution ranges) and that all species experienced recent population growth. A lack of phylogeographic structure in the two eupelagic species, Bathybates fasciatus and B. leo, was consistent with expectations and with findings in other pelagic cichlid species. Contrary to expectations, a clear phylogeographic structure was detected in the two benthopelagic species, B. graueri and Hemibates stenosoma. Differences in genetic diversity between eupelagic and benthopelagic species may be due to differences in their dispersal propensity, mediated by their respective predatory niches, rather than precipitated by external barriers to dispersal.Peer reviewe

Description and ecophysiology of a new species of Syndesmis Silliman, 1881 (Rhabdocoela: Umagillidae) from the sea urchin Evechinus chloroticus (Valenciennes, 1846) Mortensen, 1943 in New Zealand

A new rhabdocoel of the genus Syndesmis Silliman, 1881 (Umagillidae) is described from the intestine of the New Zealand sea urchin Evechinus chloroticus (Valenciennes, 1846) Mortensen, 1943a. This new species, Syndesmis kurakaikina n. sp., is morphologically distinct and can easily be recognised by its very long (+/- 1 mm) styles and its bright-red colour. In addition to providing a formal description, we present some observations on reproduction and life history of this new species. Fecundity is comparable to that of other umagillids and the rate of egg production and development increases with temperature. Hatching in this species is induced by intestinal fluids of its host. Relevant to global warming, we assessed the effect of temperature on survival, fecundity, and development. The tests indicate that Syndesmis kurakaikina n. sp. is tolerant of a wide range of temperatures (11-25 degrees C) and that its temperature optimum lies between 18.0 and 21.5 degrees C. Egg viability is, however, significantly compromised at the higher end of this temperature range, with expelled egg capsules often being deformed and showing increasingly lower rates of hatching. Given this, a rise in global temperature might increase the risk of Syndesmis kurakaikina n. sp. infecting new hosts and would possibly facilitate the spread of these endosymbionts.Peer reviewe

The Monogenean Parasite Fauna of Cichlids: A Potential Tool for Host Biogeography

We discuss geographical distribution and phylogeny of Dactylogyridea (Monogenea) parasitizing Cichlidae to elucidate their hosts' history. Although mesoparasitic Monogenea (Enterogyrus spp.) show typical vicariant distribution, ectoparasitic representatives from different continents are not considered sister taxa, hence their distribution cannot result from vicariance alone. Because of the close host-parasite relationship, this might indicate that present-day cichlid distribution may also reflect dispersal through coastal or brackish waters. Loss of ectoparasites during transoceanic migration, followed by lateral transfer from other fish families might explain extant host-parasite associations. Because of its mesoparasitic nature, hence not subject to salinity variations of the host's environment, Enterogyrus could have survived marine migrations, intolerable for ectoparasites. Host-switches and salinity transitions may be invoked to explain the pattern revealed by a preliminary morphological phylogeny of monogenean genera from Cichlidae and other selected Monogenea genera, rendering the parasite distribution explicable under both vicariance and dispersal. Testable hypotheses are put forward in this parasitological approach to cichlid biogeography. Along with more comprehensive in-depth morphological phylogeny, comparison with molecular data, clarifying dactylogyridean evolution on different continents and from various fish families, and providing temporal information on host-parasite history, are needed to discriminate between the possible scenarios

Toward a Global Phylogeny of the “Living Fossil" Crustacean Order of the Notostraca

Tadpole shrimp (Crustacea, Notostraca) are iconic inhabitants of temporary aquatic habitats worldwide. Often cited as prime examples of evolutionary stasis, surviving representatives closely resemble fossils older than 200 mya, suggestive of an ancient origin. Despite significant interest in the group as ‘living fossils’ the taxonomy of surviving taxa is still under debate and both the phylogenetic relationships among different lineages and the timing of diversification remain unclear. We constructed a molecular phylogeny of the Notostraca using model based phylogenetic methods. Our analyses supported the monophyly of the two genera Triops and Lepidurus, although for Triops support was weak. Results also revealed high levels of cryptic diversity as well as a peculiar biogeographic link between Australia and North America presumably mediated by historic long distance dispersal. We concluded that, although some present day tadpole shrimp species closely resemble fossil specimens as old as 250 mya, no molecular support was found for an ancient (pre) Mesozoic radiation. Instead, living tadpole shrimp are most likely the result of a relatively recent radiation in the Cenozoic era and close resemblances between recent and fossil taxa are probably the result of the highly conserved general morphology in this group and of homoplasy

Six new species of Cichlidogyrus Paperna, 1960 (Platyhelminthes: Monogenea) from the gills of cichlids (Teleostei: Cichliformes) from the Lomami River Basin (DRC: Middle Congo)

Background Monogenea van Beneden, 1858 is a group of parasitic flatworms, commonly found infecting bony fish. Several genera, such as Cichlidogyrus Paperna, 1960, are reported to include potential pathogenic species that can negatively impact aquaculture fish stocks. They can switch from introduced to native fish and vice versa. In Africa (and all over the world), fish species belonging to Cichlidae are often kept in aquaculture and represent a major source of food. Thus, research on the biodiversity and occurrence of monogenean species on these fish is of importance for aquaculture and conservation. The present study is a survey of the diversity of species of Cichlidogyrus in the south of the Democratic Republic of the Congo (DRC) on three cichlid species: Orthochromis sp. 'Lomami', Serranochromis cf. macrocephalus, and Tilapia sparrmanii Smith, 1840. Methods Specimens of Cichlidogyrus were isolated from the gills and mounted on glass slides with Hoyer's medium. The genital and haptoral hard parts were measured and drawn using interference contrast. Results In total, six species of Cichlidogyrus were found, all new to science: C. bulbophallus n. sp. and C. pseudozambezensis n. sp. on S. cf. macrocephalus, C. flagellum n. sp. and C. lobus n. sp. on T. sparrmanii, C. ranula n. sp. on S. cf. macrocephalus and Orthochromis sp. 'Lomami', and C. maeander n. sp. found on Orthochromis sp. 'Lomami' and T. sparrmanii. The first four species are considered to be strict specialists, C. ranula n. sp. an intermediate generalist and C. maeander n. sp. a generalist. These parasite species show morphological similarities to species found in the Lower Guinea and Zambezi ichthyofaunal provinces, which might be explained by past river capture events between river systems of the Congo Province and both these regions. Conclusions Serranochromis cf. macrocephalus and Orthochromis sp. 'Lomami' can harbour respectively three and two species of Cichlidogyrus, all described in this study. Tilapia sparrmanii can harbour seven species, of which three are described in the present study. These results highlight the species diversity of this parasite genus in the Congo Basin.Peer reviewe

Uncharted digenean diversity in Lake Tanganyika : cryptogonimids (Digenea: Cryptogonimidae) infecting endemic lates perches (Actinopterygii: Latidae)

Background Lake Tanganyika is considered a biodiversity hotspot with exceptional species richness and level of endemism. Given the global importance of the lake in the field of evolutionary biology, the understudied status of its parasite fauna is surprising with a single digenean species reported to date. Although the most famous group within the lake's fish fauna are cichlids, the pelagic zone is occupied mainly by endemic species of clupeids (Actinopterygii: Clupeidae) and lates perches (Actinopterygii: Latidae, Lates Cuvier), which are an important commercial source for local fisheries. In this study, we focused on the lake's four lates perches and targeted their thus far unexplored endoparasitic digenean fauna. Methods A total of 85 lates perches from four localities in Lake Tanganyika were examined. Cryptogonimid digeneans were studied by means of morphological and molecular characterisation. Partial sequences of the nuclear 28S rRNA gene and the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene were sequenced for a representative subset of the specimens recovered. Phylogenetic analyses were conducted at the family level under Bayesian inference. Results Our integrative approach revealed the presence of six species within the family Cryptogonimidae Ward, 1917. Three out of the four species of Lates were found to be infected with at least one cryptogonimid species. Two out of the three reported genera are new to science. Low interspecific but high intraspecific phenotypic and genetic diversity was found among Neocladocystis spp. Phylogenetic inference based on partial 28S rDNA sequences revealed a sister group relationship for two of the newly erected genera and their close relatedness to the widely distributed genus Acanthostomum Looss, 1899. Conclusions The present study provides the first comprehensive characterisation of the digenean diversity in a fish family from Lake Tanganyika which will serve as a baseline for future explorations of the lake's digenean fauna. Our study highlights the importance of employing an integrative approach for revealing the diversity in this unique host-parasite system.Peer reviewe

Monogenean parasites of sardines in Lake Tanganyika : diversity, origin and intraspecific variability

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Amended diagnosis, mitochondrial genome, and phylogenetic position of Sphyranura euryceae (Neodermata, Monogenea, Polystomatidae), a parasite of the Oklahoma salamander

Polystomatidae is a monogenean family whose representatives infect mainly (semi)-aquatic tetrapods. Species of Sphyranura Wright, 1879 exhibit ectoparasitism on salamander hosts, with molecular work supporting their inclusion within Polystomatidae, at an early diverging, yet unresolved, position in the clade of otherwise endoparasitic polystomatid parasites of batrachian hosts. Records of representatives of Sphyranura are scarce with genetic data only available for S. oligorchis Alvey, 1933. Based on detailed morphological examination and comparison with type material, we identified worms belonging to Sphyranura infecting Oklahoma salamander (Eurycea tynerensis) as S. euryceae Hughes & Moore, 1943. Along with an amended diagnosis of Sphyranura, we provide the first molecular data for S. euryceae in the form of a mitochondrial genome and nuclear (18S, 28S rRNA) markers. Close morphological similarity between the two species of Sphyranura is reflected in low genetic divergence. Mitochondrial level comparison reveals instances of tRNA gene rearrangements in polystomatids. Although the phylogenetic reconstruction supports Sphyranura as early branching in the lineage of polystomatid monogeneans infecting batrachians, certain nodes remain unresolved