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Tanglegram of Thaparocleidus and Pangasiidae species deduced from comparison of parasite tree inferred from combined data of 18S rDNA and ITS1 sequences and the fish tree obtained from cytochrome b analyses. P-values resulting from Parafit for significant host-parasite links are included.
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The phylogeny of monogeneans of the genus Thaparocleidus that parasitize the gills of Pangasiidae in Borneo and Sumatra was inferred from molecular data to investigate parasite speciation. The phylogeny of the Pangasiidae was also reconstructed in order to investigate host-parasite coevolutionary history. The monophyly of Thaparocleidus parasitizin...
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Citations
... The best-fitting model of molecular evolution was selected for each gene dataset using ModelFinder [68]. According to the Bayesian information criterion (BIC), the TVM + F + I + G model was selected as the most appropriate evolutionary model for the 18S dataset, the TVM + F + I + G model for the ITS1 dataset, the TNe + G model for the 5 [69], employing the best fit substitution model (see above) and a sub-tree pruning and re-grafting (SPR) branch-swapping algorithm. Branch support (bootstrap support, BS) was estimated using ultrafast bootstrap approximation [70] with 1000 replicates. ...
Knowledge on the diversity of parasitic flatworms of Western Mediterranean cyprinids is extremely scarce. In the present study, we parasitologically investigated 12 cyprinid species across the Strait of Gibraltar inhabiting watersheds in northwest Africa (Morocco) and Iberia (Portugal and Spain). Taxonomically relevant features of the attachment organ and sequences of the 18S rDNA and ITS regions were used for species delineation and to investigate their phylogenetic relatedness. Among the Gyrodactylus collected from Morocco and Spain, we identified specimens with an unusual T-shaped dorsal bar observed herein for the first time. In contrast, the membranous patch-like structure surrounding the twisted inner roots of hamuli and the median ridge of the ventral bar have been generally observed in Eurasian relatives. Our analyses suggest vicariant speciation of Gyrodactylus across the Strait of Gibraltar. We describe herein G. gibraltarensis sp. nov. from Iberian Luciobarbus graellsii; G. moroccensis sp. nov. from northwest African cyprinids, i.e., L. maghrebensis, L. rabatensis, L. rifensis, L. yahyaouii, and L. zayanensis; and finally, G. pseudomoroccensis sp. nov. from Moroccan L. ksibi, all possessing a new haptoral configuration. The genetic divergence and conservative morphologies in populations of G. moroccensis sp. nov. from five cyprinid species support its ongoing speciation in Northwest Africa. The West Mediterranean lineage was revealed to be monophyletic, with Eurasian species forming a sister group. Morphologically, West Mediterranean Gyrodactylus also appeared to be of Middle Eastern origin. Gyrodactylus spp. possessing an unusual T-shaped dorsal bar have most likely speciated, allowing for the appearance of a haptoral morphology that is restricted to the region across the Strait of Gibraltar. To conclude, viviparous Gyrodactylus reflect parasite speciation across the Strait of Gibraltar and the historical biogeography of cyprinids in the West Mediterranean.
... Most monogenean genera are specific to a group of related host species; for example, Dactylogyrus is found on cyprinids, Cichlidogyrus on cichlids, while catfish harbour Thaparocleidus (see Shaharom, 1985). Although at species level most monogeneans are specific to a particular host, some, like Thaparocleidus caecus, are found on several pangasiids (Lim et al., 2001;Šimková et al., 2013). ...
... Species belonging to this monogenean genus are found on cultured pangasiids and bagrids in South-East Asia (see Pariselle et al., 2002;Thuy and Buchmann, 2008;Šimková et al., 2013;Lio-Po and Lim, 2014) (Fig. 6.8F). As with Pseudodactylogyroides, little is known about the pathology caused by this group of monogeneans, or the level of pathogenicity. ...
... The diversification of a particular parasite is expected to be intimately linked with the diversification of the respective host taxon, which can be reflected in hostparasite cospeciation. Nonetheless, recent studies (e.g., Desdevises et al., 2002;Huyse and Volckaert, 2005;Š imková et al., 2013;Míguez-Lozano et al., 2017;Benovics et al., 2020c) have shown that speciation in the monogeneans is far more complex and is driven by a combination of coevolutionary events; i.e., host-switching or intra-host duplication (see the review by Niebering and Olivieri (2007) for individual cophylogenetic events). ...
Host-parasite coevolution is one of the fundamentals of evolutionary biology. Due to the intertwined evolutionary history of two interacting species and reciprocal coadaptation processes of hosts and parasites, we can expect that studying parasites will shed more light onto the evolutionary processes of their hosts. Monogenea (ectoparasitic Platyhelminthes) and their cyprinoid fish hosts represent one of the best models for studying host-parasite evolutionary relationships using a cophylogenetic approach. These parasites have developed remarkably high host specificity, where each host species often serves as a potential host for its own host-specific monogenean species. Here, the cophylogenetic relationships in the Dactylogyrus-Squalius system was investigated, as Squalius is one of several cyprinoid genera with puzzling phylogeography and inhabits all four major peri-Mediterranean peninsulas. Of 29 endemic Squalius species examined for the presence of Dactylogyrus parasites, a total of 13 Dactylogyrus species were collected from the gills of 20 Squalius species across a wide range of distribution. Phylogenetic reconstruction revealed a polyphyletic origin for Dactylogyrus species parasitizing congeneric Squalius, with four major clades being recognized. On the basis of the delimitation of host specificity, strict specialists parasitizing single host species, geographic specialists parasitizing congeners in a limited geographical region, and true generalists parasitizing congeners in various geographical regions were recognized in Dactylogyrus species parasitizing Squalius. The phylogenetic reconstruction of Squalius hosts revealed two major clades, the first encompassing only peri-Mediterranean species and the second including species from other Euro-Asian regions. Distance-based cophylogenetic methods did not reveal a statistically significant global cophylogenetic structure in the studied system; however, several host-parasite links among Iberian endemic species contributed significantly to the overall structure. The widest host range and associated genetic variability were recorded for D. folkmanovae, parasitizing nine Squalius species, and D. vistulae, parasitizing 13 Squalius species. Two different dispersion mechanisms and morphological adaptations to Squalius hosts were clearly reflected in the contrasting cophylogenetic patterns for these two species with different levels of host specificity. While host-parasite cospeciation plays an important role in diversification within D. folkmanovae, diversification within D. vistulae is driven mainly by host switching.
... Species of Cichlidogyrus rival (Cruz-Laufer et al., 2021) and possibly exceed (see Poulin, 2014) their hosts in terms of species numbers: 137 parasite species have been described on 126 fish species (Cruz-Laufer et al., 2021). Monogenean flatworms have provided insight into parasite speciation (Meinil€ a et al., 2004;Simkov a et al., 2013;, population dynamics (Kmentov a et al., 2021), anthropogenic introductions (Jorissen et al., 2020;Simkov a et al., 2019) and host biogeography (Barson et al., 2010;Pariselle et al., 2011;Vanhove et al., 2013Vanhove et al., , 2016. These gill parasites are well-shielded from external physical forces by the gill flaps and are, therefore, found on many specimens in historical museum collections as by-products of host samplings (Jorissen et al., 2020). ...
... Species of Cichlidogyrus rival (Cruz-Laufer et al., 2021) and possibly exceed (see Poulin, 2014) their hosts in terms of species numbers: 137 parasite species have been described on 126 fish species (Cruz-Laufer et al., 2021). Monogenean flatworms have provided insight into parasite speciation (Meinil€ a et al., 2004;Simkov a et al., 2013;, population dynamics (Kmentov a et al., 2021), anthropogenic introductions (Jorissen et al., 2020;Simkov a et al., 2019) and host biogeography (Barson et al., 2010;Pariselle et al., 2011;Vanhove et al., 2013Vanhove et al., , 2016. These gill parasites are well-shielded from external physical forces by the gill flaps and are, therefore, found on many specimens in historical museum collections as by-products of host samplings (Jorissen et al., 2020). ...
... Fish specimens belonging to Cichlidae Bonaparte, 1835 (Cichliformes), the nothobranchiid genus Aphyosemion Myers, 1924 (Cyprinodontiformes: Nothobranchiidae), and Polycentropsis abbreviata Boulenger, 1901 (Ovalentaria, incertae sedis: Polycentridae) were collected across Africa (and from aquaculture facilities in France) between 2008 and 2019 (Appendix 1). As these samples have been included in previous studies, sampling details can be found elsewhere (Jorissen et al., , 2020Muterezi Bukinga et al., 2012;Pariselle et al., 2015aPariselle et al., , 2015bVanhove et al., , 2013. Gills were dissected and stored in 96% ethanol to preserve parasite DNA. ...
A substantial portion of biodiversity has evolved through adaptive radiation. However, the effects of explosive speciation on species interactions remain poorly understood. Metazoan parasites infecting radiating host lineages could improve our knowledge because of their intimate host relationships. Yet limited molecular, phenotypic and ecological data discourage multivariate analyses of evolutionary patterns and encourage the use of discrete characters. Here, we assemble new molecular, morphological and host range data widely inferred from a species‐rich lineage of parasites (Cichlidogyrus, Platyhelminthes: Monogenea) infecting cichlid fishes to address data scarcity. We infer a multimarker (28S/18S rDNA, ITS1, COI mtDNA) phylogeny of 58 of 137 species and characterize major lineages through synapomorphies inferred from mapping morphological characters. We predict the phylogenetic position of species without DNA data through shared character states, a morphological phylogenetic analysis, and a classification analysis with support vector machines. Based on these predictions and a cluster analysis, we assess the systematic informativeness of continuous characters, search for continuous equivalents for discrete characters, and suggest new characters for morphological traits not analysed to date. We also model the attachment/reproductive organ and host range evolution using the data for 136 of 137 described species and multivariate phylogenetic comparative methods (PCMs). We show that discrete characters not only can mask phylogenetic signals, but also are key for characterizing species groups. Regarding the attachment organ morphology, a divergent evolutionary regime for at least one lineage was detected and a limited morphological variation indicates host and environmental parameters affecting its evolution. However, moderate success in predicting phylogenetic positions, and a low systematic informativeness and high multicollinearity of morphological characters call for a revaluation of characters included in species characterizations.
... Haliotrema Johnston & Tiegs, 1922;Euryhaliotrema Kritsky & Boeger, 2002;Haliotrematoides Kritsky, Yang & Sun, 2009;and Pseudempleurosoma Yamaguti, 1965) through analyses of the small subunit (SSU) and LSU of the rRNA gene (Plaisance et al., 2005;Wu et al., 2007;Dang et al., 2010;Garcia-Vasquez et al., 2015;Mendoza-Palmero et al., 2015;Theisen et al., 2017Theisen et al., , 2018. The internal transcribed spacer region 1 (ITS1) was also used to explore the intraspecific variability (Š imková et al., 2004;Stefani et al., 2012;Š imková et al., 2013;Kmentová et al., 2015). ...
A new ancyrocephalid monogenean is described from the gills of wild White-spottedrabbitfish Siganus canaliculatus (Park) based on morphological and molecular analyses. Glyphidohaptor safiensis n. sp. can be distinguished from other members of the genus by the shape of the accessory piece of the male copulatory organ (MCO). Unlike its congeners, the rod-shaped accessory piece of G. safiensis n. sp. is distally broad and flattened. The MCO of G. safiensis n. sp. is curved, enclosed in a heavy sheath with a terminal flap. Partial large subunit (LSU), partial small subunit (SSU) and the partial SSU, entire internal transcribed spacer region 1 (ITS1) and partial 5.8S rDNA of the new species and two species of Tetrancistrum Goto & Kikuchi, 1917 from the same host and locality were sequenced and subjected to phylogenetic analysis. The LSU rDNA analysis grouped G. safiensis n. sp. with Tetrancistrum sp. from the gills of Siganus fuscescens Houttuyn from Australia, indicating a possible misidentification of the latter. Sequences of the SSU rDNA of the new species were most similar to those for Pseudohaliotrema sphincteroporus Yamaguti, 1953, demonstrating the close relatedness of the genera Pseudohaliotrema Yamaguti, 1953 and Glyphidohaptor Kritsky, Galli & Yang, 2007 within the Ancyrocephalidae. The comparison of the partial SSU (424 bp) and entire ITS1 and partial 5.8S rDNA (246 bp) sequences obtained for G. safiensis n. sp. with the only available sequence of another member of Glyphidohaptor Kritsky, Galli & Yang, 2007, G. pletocirra Paperna, 1972 (HE601931-HE601933) yielded on average 1.08% dissimilarity (a difference of 7 bases), with a p-distance of 0.010 ± 0.004%. This is the first record of a species of Glyphidohaptor from S. canaliculatus and from the Persian Gulf, the Gulf of Oman and the Arabian Sea.
... However, the whole concept of the 'Fahrenholz rule' has been re-evaluated and several studies have suggested that cospeciation is not always the predominant driver of parasite speciation during reciprocal host-parasite evolution. Host switching (Klassen, 1992) and parasite duplication, that is parasite speciation within a host lineage (Johnson, Adams, Page, & Clayton, 2003), play significant roles in parasite evolution, often resulting in incongruent host and parasite phylogenies (Desdevises, Morand, Jousson, & Legendre, 2002;Mendlová, Desdevides, Civáňová, Pariselle, & Šimková, 2012;Šimková, Morand, Jobet, Gelnar, & Verneau, 2004;Šimková, Serbielle, Pariselle, Vanhove, & Morand, 2013). Despite the fact that frequent host switching during the evolutionary history of parasite taxa usually results in incongruent host-parasite phylogenies, a series of multiple host switches followed by parasite speciation can generate trees with similar topologies (de Vienne, Giraud, & Shykoff, 2007). ...
The study of host–parasite coevolution is one of the cornerstones of evolutionary biology. The majority of fish ectoparasites belonging to the genus Dactylogyrus (Monogenea) exhibit a high degree of host specificity. Therefore, it is expected that their evolutionary history is primarily linked with the evolutionary history of their cyprinoid fish hosts and the historical formation of the landmasses. In the present study, we used a cophylogenetic approach to investigate coevolutionary relationships between endemic Cyprinoidea (Cyprinidae and Leuciscidae) from selected regions in southern Europe and their respective Dactylogyrus species. A total of 49 Dactylogyrus species including endemic and non‐endemic species were collected from 62 endemic cyprinoid species in the Balkan and Apennine Peninsulas. However, 21 morphologically identified Dactylogyrus species exhibited different genetic variants (ranging from 2 to 28 variants per species) and some of them were recognized as cryptic species on the basis of phylogenetic reconstruction. Phylogenetic analyses revealed several lineages of endemic and non‐endemic Dactylogyrus species reflecting some morphological similarities or host affinities. Using distance‐based and event‐based cophylogenetic methods, we found a significant coevolutionary signal between the phylogenies of parasites and their hosts. In particular, statistically significant links were revealed between Dactylogyrus species of Barbini (Cyprinidae) and their hosts belonging to the genera Aulopyge, Barbus and Luciobarbus. Additionally, a strong coevolutionary link was found between the generalist parasites D. alatus, D. sphyrna, D. vistulae, and their hosts, and between Dactylogyrus species of Pachychilon (Leuciscidae) and their hosts. Cophylogenetic analyses suggest that host switching played an important role in the evolutionary history of Dactylogyrus parasitizing endemic cyprinoids in southern Europe. We propose that the high diversification of phylogenetically related cyprinoid species in the Mediterranean area is a process facilitating the host switching of specific parasites among highly diverse congeneric cyprinoids. We used the cophylogenetic approach to investigate coevolutionary relationships between endemic cyprinoids from the Apennine and Balkan Peninsulas, and their respective Dactylogyrus species. Using distance‐based and event‐based cophylogenetic methods, we found significant coevolutionary signal between phylogenies of the parasites and hosts. Out of 138 host‐parasite individual links, 65 contributed significantly to the global cophylogenetic structure (p < .05). Results of the event‐based cophylogenetic analyses suggest that Dactylogyrus speciation is primarily driven by duplication followed by host‐switching.
... Though it was successfully used for differentiation of two age stages in Polystomatidae (Rubtsova & Heckmann, 2017), it was never carried out for different gallium cuts of the anchors in Monogenea, accomplished with SEM. In the present study, we provide metric parameters according to Gusev (1985) that now are widely used in studies of Monogenea (Šimková et al., 2013;Acosta et al., 2018). For instance, "complete anchor length" in Ergens (1966) is what was later accepted as ventroapical length (for four-anchored monogeneans) (Gusev, 1985). ...
New morphometric data, including details of the copulatory system and attachment structures, as well as inner organs are provided for Ancyrocephalus paradoxus Creplin, 1839. Scanning electron microscopy reveals new information of the body shape, position of the cephalic organs' openings, and structure of anchors, as well as differences in the in anchors' structure in adults and sub-adults of A. paradoxus. Energy dispersive analysis for X-ray was conducted for the fi rst time for anchors in Monogenea and revealed structural differences between different parts of the anchors in two age groups.
... Therefore, we suspect a possibility of the existence of a cryptic Eudiplozoon species. Further investigations of the Eudiplozoon population in Tangxun Lake are needed to establish whether the unusually low identities of ITS-2 and cox1 sequences are a reflection of the existence of a cryptic species, as intrahost or sympatric speciation is more likely in monogeneans than in other parasitic groups [35][36][37], or merely an unusually high mutational rate of genomes (both nuclear and mitochondrial) of some sub-populations. ...
Background
As the topologies produced by previous molecular and morphological studies were contradictory and unstable (polytomy), evolutionary relationships within the Diplozoidae family and the Monogenea class (controversial relationships among the Discocotylinea, Microcotylinea and Gastrocotylinea suborders) remain unresolved. Complete mitogenomes carry a relatively large amount of information, sufficient to provide a much higher phylogenetic resolution than traditionally used morphological traits and/or single molecular markers. However, their implementation is hampered by the scarcity of available monogenean mitogenomes. Therefore, we sequenced and characterized mitogenomes belonging to three Diplozoidae family species, and conducted comparative genomic and phylogenomic analyses for the entire Monogenea class.
Results
Taxonomic identification was inconclusive, so two of the species were identified merely to the genus level. The complete mitogenomes of Sindiplozoon sp. and Eudiplozoon sp. are 14,334 bp and 15,239 bp in size, respectively. Paradiplozoon opsariichthydis (15,385 bp) is incomplete: an approximately 2000 bp-long gap within a non-coding region could not be sequenced. Each genome contains the standard 36 genes (atp8 is missing). G + T content and the degree of GC- and AT-skews of these three mitogenome (and their individual elements) were higher than in other monogeneans. nad2, atp6 and nad6 were the most variable PCGs, whereas cox1, nad1 and cytb were the most conserved. Mitochondrial phylogenomics analysis, conducted using concatenated amino acid sequences of all PCGs, indicates that evolutionary relationships of the three genera are: (Eudiplozoon, (Paradiplozoon, Sindiplozoon)); and of the three suborders: (Discocotylinea, (Microcotylinea, Gastrocotylinea)). These intergeneric relationships were also supported by the skewness and principal component analyses.
Conclusions
Our results show that nad2, atp6 and nad6 (fast-evolving) would be better candidates than cox1 (slow-evolving) for species identification and population genetics studies in Diplozoidae. Nucleotide bias and codon and amino acid usage patterns of the three diplozoid mitogenomes are more similar to cestodes and trematodes than to other monogenean flatworms. This unusual mutational bias was reflected in disproportionately long branches in the phylogram. Our study offsets the scarcity of molecular data for the subclass Polyopisthocotylea to some extent, and might provide important new insights into the evolutionary history of the three genera and three suborders.
... Within H. vittatus, three well-supported, previously unrecognized lineages were recovered by these authors. Inasmuch as the natural classification of some parasite groups usually corresponds directly with the natural relationships of their hosts (Eichler, 1948;Mendlová et al., 2012;Šimková et al., 2013), it will be interesting to see whether and how community structures of the Annulotrema species infesting African tigerfishes vary with geographic location. Thus, broader sampling of tigerfishes and further analysis (utilizing both morphological and molecular data) are required to provide more detailed resolution on the relationships between monogeneans and their Hydrocynus hosts across Africa. ...
Two new and one known species of Annulotrema Paperna & Thurston, 1969 are reported from the gills of the tigerfish Hydrocynus vittatus Castelnau, 1861, collected in Lake Kariba, Zimbabwe. The new species, Annulotrema pseudonili n. sp. and A. bracteatum n. sp., are described and distinguished mainly on the basis of features of the male copulatory organ (MCO). Annulotrema pseudonili n. sp. most closely resembles A. nili Paperna, 1973, but differs from it by possessing a more delicate MCO with a thin-walled base without a fibrous distal part. Annulotrema bracteatum n. sp. is most similar to Annulotrema ruahae Paperna, 1973, from which it differs by having an MCO composed of a longer copulatory tube and a leaf-shaped accessory piece enveloping the distal part of the tube. The presence of Annulotrema pikoides Guégan, Lambert & Birgi, 1988 on H. vittatus in Zimbabwe represents a new locality record for this parasite.
... In fact, different coevolutionary studies of monogeneans and their fish hosts, such as Lamellodiscus on Sparidae (4), Thaparocleidus on Pangasiidae [21], Cichlidogyrus on Cichlidae [22][23][24], Dactylogyrus on Cyprinidae [25,26], and Gyrodactylus on Gobiidae [27] and Salmonidae [28], have shown that host switching and duplication are the most important evolutionary events in parasite diversification and that cospeciation is relatively rare in these host-parasite systems [4,22]. ...
Cophylogenetic studies aim at testing specific hypotheses to understand the nature of coevolving associations between sets of organisms, such as host and parasites. Monogene-ans and their hosts provide and interesting platform for these studies due to their high host specificity. In this context, the objective of the present study was to establish whether the relationship between Anacanthorus spp. with their hosts from the upper Paraná River and its tributaries can be explained by means of cospeciation processes. Nine fish species and 14 monogenean species, most of them host specific, were studied. Partial DNA sequences of the genes RAG1, 16S and COI of the fish hosts and of the genes ITS2, COI and 5.8S of the parasite species were used for phylogenetic reconstruction. Maximum likelihood phylo-genetic trees of the host and parasite species were built and used for analyses of topological congruence with PACo and ParaFit. The program Jane was used to estimate the nature of cospeciation events. The comparison of the two phylogenies revealed high topological congruence between them. Both PACo and ParaFit supported the hypothesis of global cospe-ciation. Results from Jane pointed to duplications as the most frequent coevolutionary event, followed by cospeciation, whereas duplications followed by host-switching were the least common event in Anacanthorus spp. studied. Host-sharing (spreading) was also identified but only between congeneric host species.
