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

publishedVersio

Weak population structure and recent demographic expansion of the monogenean parasite Kapentagyrus spp. infecting clupeid fishes of Lake Tanganyika, East Africa

Author's accepted version (postprint).This is an Accepted Manuscript of an article published by Elsevier in International Journal for Parasitology on 08/04/2020.Available online: https://www.sciencedirect.com/science/article/pii/S0020751920300606?via%3DihubLake Tanganyika, East Africa, is the oldest and deepest African Great Lake and harbours one of the most diverse fish assemblages on earth. Two clupeid fishes, Limnothrissa miodon and Stolothrissa tanganicae, constitute a major part of the total fish catch, making them indispensable for local food security. Parasites have been proposed as indicators of stock structure in highly mobile pelagic hosts. We examined the monogeneans Kapentagyrus limnotrissae and Kapentagyrus tanganicanus (Dactylogyridae) infecting these clupeids to explore the parasites’ lake-wide population structure and patterns of demographic history. Samples were collected at seven sites distributed across three sub-basins of the lake. Intraspecific morphological variation of the monogeneans (n = 380) was analysed using morphometrics and geomorphometrics of sclerotised structures. Genetic population structure of both parasite species (n = 246) was assessed based on a 415 bp fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene. Overall, we observed a lack of clear geographical morphological differentiation in both parasites along a north–south axis. This lack of geographical population structure was also reflected by a large proportion of shared haplotypes, and a pattern of seemingly unrestricted gene flow between populations. Significant morphological and genetic differentiation between some populations might reflect temporal differentiation rather than geographical isolation. Overall, the shallow population structure of both species of Kapentagyrus reflects the near-panmictic population structure of both host species as previously reported. Morphological differences related to host species identity of K. tanganicanus were consistent with incipient speciation at the genetic level. Both parasite species experienced a recent demographic expansion, which might be linked to paleohydrological events. Finally, interspecific hybridisation was found in Kapentagyrus, representing the first case in dactylogyrid monogeneans.acceptedVersio

Architecture of Paradiplozoon homoion: A diplozoid monogenean exhibiting highly-developed equipment for ectoparasitism.

Diplozoidae (Monogenea) are blood-feeding freshwater fish gill ectoparasites with extraordinary body architecture and a unique sexual behaviour in which two larval worms fuse and transform into one functioning individual. In this study, we describe the body organisation of Paradiplozoon homoion adult stage using a combined approach of confocal laser scanning and electron microscopy, with emphasis on the forebody and hindbody. Special attention is given to structures involved in functional adaptation to ectoparasitism, i.e. host searching, attachment and feeding/metabolism. Our observations indicate clear adaptations for blood sucking, with a well-innervated mouth opening surrounded by sensory structures, prominent muscular buccal suckers and a pharynx. The buccal cavity surface is covered with numerous tegumentary digitations that increase the area in contact with host tissue and, subsequently, with its blood. The buccal suckers and the well-innervated haptor (with sclerotised clamps controlled by noticeable musculature) cooperate in attaching to and moving over the host. Putative gland cells accumulate in the region of apical circular structures, pharynx area and in the haptor middle region. Paired club-shaped sacs lying laterally to the pharynx might serve as secretory reservoirs. Furthermore, we were able to visualise the body wall musculature, including peripheral innervation, the distribution of uniciliated sensory structures essential for reception of external environmental information, and flame cells involved in excretion. Our results confirm in detail that P. homoion displays a range of sophisticated adaptations to an ectoparasitic life style, characteristic for diplozoid monogeneans

Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish.

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

First insights into the diversity of gill monogeneans of ‘Gnathochromis’ and Limnochromis (Teleostei, Cichlidae) in Burundi: do the parasites mirror host ecology and phylogenetic history?

Monogenea is one of the most species-rich groups of parasitic flatworms worldwide, with many species described only recently, which is particularly true for African monogeneans. For example, Cichlidogyrus, a genus mostly occurring on African cichlids, comprises more than 100 nominal species. Twenty-two of these have been described from Lake Tanganyika, a famous biodiversity hotspot in which many vertebrate and invertebrate taxa, including monogeneans, underwent unique and spectacular radiations. Given their often high degrees of host specificity, parasitic monogeneans were also used as a potential tool to uncover host species relationships. This study presents the first investigation of the monogenean fauna occurring on the gills of endemic 'Gnathochromis' species along the Burundese coastline of Lake Tanganyika. We test whether their monogenean fauna reflects the different phylogenetic position and ecological niche of 'Gnathochromis' pfefferi and Gnathochromis permaxillaris. Worms collected from specimens of Limnochromis auritus, a cichlid belonging to the same cichlid tribe as G. permaxillaris, were used for comparison. Morphological as well as genetic characterisation was used for parasite identification. In total, all 73 Cichlidogyrus individuals collected from 'G.' pfefferi were identified as C. irenae. This is the only representative of Cichlidogyrus previously described from 'G.' pfefferi, its type host. Gnathochromis permaxillaris is infected by a species of Cichlidogyrus morphologically very similar to C. gillardinae. The monogenean species collected from L. auritus is considered as new for science, but sample size was insufficient for a formal description. Our results confirm previous suggestions that 'G.' pfefferi as a good disperser is infected by a single monogenean species across the entire Lake Tanganyika. Although G. permaxillaris and L. auritus are placed in the same tribe, Cichlidogyrus sp. occurring on G. permaxillaris is morphologically more similar to C. irenae from 'G.' pfefferi, than to the Cichlidogyrus species found on L. auritus. Various evolutionary processes, such as host-switching or duplication events, might underlie the pattern observed in this particular parasite-host system. Additional samples for the Cichlidogyrus species occuring on G. permaxillaris and L. auritus are needed to unravel their evolutionary history by means of (co-)phylogenetic analyses.status: publishe

First insights into the diversity of gill monogeneans of ‘Gnathochromis’ and Limnochromis (Teleostei, Cichlidae) in Burundi: do the parasites mirror host ecology and phylogenetic history?

Monogenea is one of the most species-rich groups of parasitic flatworms worldwide, with many species described only recently, which is particularly true for African monogeneans. For example, Cichlidogyrus, a genus mostly occurring on African cichlids, comprises more than 100 nominal species. Twenty-two of these have been described from Lake Tanganyika, a famous biodiversity hotspot in which many vertebrate and invertebrate taxa, including monogeneans, underwent unique and spectacular radiations. Given their often high degrees of host specificity, parasitic monogeneans were also used as a potential tool to uncover host species relationships. This study presents the first investigation of the monogenean fauna occurring on the gills of endemic ‘Gnathochromis’ species along the Burundese coastline of Lake Tanganyika. We test whether their monogenean fauna reflects the different phylogenetic position and ecological niche of ‘Gnathochromis’ pfefferi and Gnathochromis permaxillaris. Worms collected from specimens of Limnochromis auritus, a cichlid belonging to the same cichlid tribe as G. permaxillaris, were used for comparison. Morphological as well as genetic characterisation was used for parasite identification. In total, all 73 Cichlidogyrus individuals collected from ‘G.’ pfefferi were identified as C. irenae. This is the only representative of Cichlidogyrus previously described from ‘G.’ pfefferi, its type host. Gnathochromis permaxillaris is infected by a species of Cichlidogyrus morphologically very similar to C. gillardinae. The monogenean species collected from L. auritus is considered as new for science, but sample size was insufficient for a formal description. Our results confirm previous suggestions that ‘G.’ pfefferi as a good disperser is infected by a single monogenean species across the entire Lake Tanganyika. Although G. permaxillaris and L. auritus are placed in the same tribe, Cichlidogyrus sp. occurring on G. permaxillaris is morphologically more similar to C. irenae from ‘G.’ pfefferi, than to the Cichlidogyrus species found on L. auritus. Various evolutionary processes, such as host-switching or duplication events, might underlie the pattern observed in this particular parasite-host system. Additional samples for the Cichlidogyrus species occuring on G. permaxillaris and L. auritus are needed to unravel their evolutionary history by means of (co-)phylogenetic analyses

Laser capture microdissection in combination with mass spectrometry: Approach to characterization of tissue-specific proteomes of Eudiplozoon nipponicum (Monogenea, Polyopisthocotylea).

Eudiplozoon nipponicum (Goto, 1891) is a hematophagous monogenean ectoparasite which inhabits the gills of the common carp (Cyprinus carpio). Heavy infestation can lead to anemia and in conjunction with secondary bacterial infections cause poor health and eventual death of the host. This study is based on an innovative approach to protein localization which has never been used in parasitology before. Using laser capture microdissection, we dissected particular areas of the parasite body without contaminating the samples by surrounding tissue and in combination with analysis by mass spectrometry obtained tissue-specific proteomes of tegument, intestine, and parenchyma of our model organism, E. nipponicum. We successfully verified the presence of certain functional proteins (e.g. cathepsin L) in tissues where their presence was expected (intestine) and confirmed that there were no traces of these proteins in other tissues (tegument and parenchyma). Additionally, we identified a total of 2,059 proteins, including 72 peptidases and 33 peptidase inhibitors. As expected, the greatest variety was found in the intestine and the lowest variety in the parenchyma. Our results are significant on two levels. Firstly, we demonstrated that one can localize all proteins in one analysis and without using laboratory animals (antibodies for immunolocalization of single proteins). Secondly, this study offers the first complex proteomic data on not only the E. nipponicum but within the whole class of Monogenea, which was from this point of view until recently neglected