Parasites exhibiting a high degree of host specificity are expected to be intimately associated with their hosts. Therefore, the evolution of host-specific parasites is at least partially shaped by the evolutionary history and distribution of such hosts. Gill ectoparasites of Dactylogyrus (Monogenea) are specific to cyprinid fish. In the present study, we investigated the evolutionary history of 47 Dactylogyrus species from the Balkan Peninsula, the Mediteranean region exhibiting the highest cyprinid diversity in Europe, and from central European cyprinids. Phylogenetic analyses revealed four well-supported clades of endemic and non-endemic Dactylogyrus spp. with four basal taxa. Endemic cyprinids with a limited distribution range were parasitized by endemic Dactylogyrus species, but some of them shared several Dactylogyrus species with central European cyprinids. Species delimitation analyses based on molecular data suggest that Dactylogyrus diversity is higher than that defined from morphology. Some endemic cyprinid species harboured Dactylogyrus species of different origins, this probably resulting from multiple host switching. Our results support the view that the evolution of Dactylogyrus in the Balkans has been influenced not only by the historical dispersion and distribution of their cyprinid hosts, but also by recent contacts of non-native cyprinid species with endemic cyprinid fauna in this region.

BackgroundHost specificity in parasites represents the extent to which a parasite’s distribution is limited to certain host species. Considering host-specific parasites of primarily freshwater fish (such as gill monogeneans), their biogeographical distribution is essentially influenced by both evolutionary and ecological processes. Due to the limited capacity for historical dispersion in freshwater fish, their specific coevolving parasites may, through historical host-parasite associations, at least partially reveal the historical biogeographical routes (or historical contacts) of host species. We used Dactylogyrus spp., parasites specific to cyprinid fish, to infer potential historical contacts between Northwest African and European and Asian cyprinid faunas. Using phylogenetic reconstruction, we investigated the origin(s) of host-specific Dactylogyrus spp. parasitizing Northwest African and Iberian cyprinid species.ResultsIn accordance with hypotheses on the historical biogeography of two cyprinid lineages in Northwest Africa, Barbini (Luciobarbus) and Torini (Carasobarbus), we demonstrated the multiple origins of Northwest African Dactylogyrus. Dactylogyrus spp. of Carasobarbus spp. originated from Asian cyprinids, while Dactylogyrus spp. of Luciobarbus spp. originated from European cyprinids. This indicates the historical Northern route of Dactylogyrus spp. dispersion to Northwest African Luciobarbus species rather than the Southern route, which is currently widely accepted for Luciobarbus. In addition, both Northwest African cyprinid lineages were also colonized by Dactylogyrus marocanus closely related to Dactylogyrus spp. parasitizing African Labeo spp., which suggests a single host switch from African Labeonini to Northwest African Luciobarbus. We also demonstrated the multiple origins of Dactylogyrus spp. parasitizing Iberian Luciobarbus species. One Iberian Dactylogyrus group was phylogenetically closely related to Dactylogyrus of Moroccan Carasobarbus, while the second was related to Dactylogyrus of Moroccan Luciobarbus.ConclusionsOur study confirms the different origins of two Northwest African cyprinid lineages. It suggests several independent historical contacts between European Iberian Luciobarbus and two lineages of Northwest African cyprinids, these contacts associated with host switches of Dactylogyrus parasites.

BackgroundThe host specificity of fish parasites is considered a useful parasite characteristic with respect to understanding the biogeography of their fish hosts. Dactylogyrus Diesing, 1850 (Monogenea) includes common parasites of cyprinids exhibiting different degrees of host specificity, i.e. from strict specialism to generalism. The phylogenetic relationships and historical dispersions of several cyprinid lineages, including Aulopyge huegelii Heckel, 1843, are still unclear. Therefore, the aims of our study were to investigate (i) the Dactylogyrus spp. parasites of A. huegelii, and (ii) the phylogenetic relationships of Dactylogyrus spp. parasitizing A. huegelii as a possible tool for understanding the phylogenetic position of this fish species within the Cyprininae lineage.ResultsTwo species of Dactylogyrus, D. vastator Nybelin, 1924 and D. omenti n. sp., were collected from 14 specimens of A. huegelii from the Šujica River (Bosnia and Herzegovina). While D. vastator is a typical species parasitizing Carassius spp. and Cyprinus carpio L, D. omenti n. sp. is, according to phylogenetic reconstruction, closely related to Dactylogyrus species infecting European species of Barbus and Luciobarbus. The genetic distance revealed that the sequence for D. vastator from A. huegelii is identical with that for D. vastator from Barbus plebejus Bonaparte, 1839 (Italy) and Carassius gibelio (Bloch, 1782) (Croatia). Dactylogyrus omenti n. sp. was described as a species new to science.ConclusionsOur findings support the phylogenetic position of A. huegelii within the Cyprininae lineage and suggest that A. huegelii is phylogenetically closely related to Barbus and Luciobarbus species. The morphological similarity between D. omenti n. sp. and Dactylogyrus species of Middle Eastern Barbus suggests historical contact between cyprinid species recently living in allopatry and the possible diversification of A. huegelii from a common ancestor in this area. On other hand, the genetic similarity between D. vastator ex A. huegelii and D. vastator ex C. gibelio collected in Balkan Peninsula suggests that A. huegelii was secondarily parasitized by D. vastator, originating from C. gibelio after introduction of this fish species from Asia to Europe.

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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

Parasite inhibitors of cysteine peptidases are known to influence a vast range of processes linked to a degradation of either the parasites’ own proteins or proteins native to their hosts. We characterise a novel type I cystatin (stefin) found in a sanguinivorous fish parasite Eudiplozoon nipponicum (Platyhelminthes: Monogenea). We have identified a transcript of its coding gene in the transcriptome of adult worms. Its amino acid sequence is similar to other stefins except for containing a legumain-binding domain, which is in this type of cystatins rather unusual. As expected, the recombinant form of E. nipponicum stefin (rEnStef) produced in Escherichia coli inhibits clan CA peptidases – cathepsins L and B of the worm – via the standard papain-binding domain. It also blocks haemoglobinolysis by cysteine peptidases in the worm’s excretory-secretory products and soluble extracts. Furthermore, we had confirmed its ability to inhibit clan CD asparaginyl endopeptidase (legumain). The presence of a native EnStef in the excretory-secretory products of adult worms, detected by mass spectrometry, suggests that this protein has an important biological function at the host-parasite interface. We discuss the inhibitor’s possible role in the regulation of blood digestion, modulation of antigen presentation, and in the regeneration of host tissues.

Background Freshwater fauna of the Middle East encompass elements shared with three continents—Africa, Asia, and Europe—and the Middle East is, therefore, considered a historical geographic crossroad between these three regions. Even though various dispersion scenarios have been proposed to explain the current distribution of cyprinids in the peri-Mediterranean, all of them congruently suggest an Asian origin for this group. Herein, we investigated the proposed scenarios using monogenean parasites of the genus Dactylogyrus, which is host-specific to cyprinoid fishes. Methods A total of 48 Dactylogyrus species parasitizing cyprinids belonging to seven genera were used for molecular phylogenetic reconstruction. Taxonomically important morphological features, i.e., sclerotized elements of the attachment organ, were further evaluated to resolve ambiguous relationships between individual phylogenetic lineages. For 37 species, sequences of partial genes coding 18S and 28S rRNA, and the ITS1 region were retrieved from GenBank. Ten Dactylogyrus species collected from Middle Eastern cyprinoids and D. falciformis were de novo sequenced for the aforementioned molecular markers. Results The phylogenetic reconstruction divided all investigated Dactylogyrus species into four phylogenetic clades. The first one encompassed species with the “varicorhini” type of haptoral ventral bar with a putative origin linked to the historical dispersion of cyprinids via the North African coastline. The second clade included the majority of the investigated species parasitizing various phylogenetically divergent cyprinid hosts. The morphological and molecular data suggest the ancestral diversification of the species of this clade into two groups: (1) the group possessing the haptoral ventral bar of the “cornu” type, and (2) the group possessing the “wunderi” type. Dactylogyrus diversification apparently occurred in the Middle East, which is indicated by the presence of species with all morphotypes in the region. The last two clades included species parasitizing cyprinids with an East Asian origin, and species possessing the “magnihamatus” type of ventral bar. Conclusions The molecular data suggest that some morphological characters of host-specific parasites may undergo convergent evolution in the divergent lineages, and therefore, to fully resolve the phylogenetic relationships among host-specific parasites, an integrative approach combining morphological and molecular data is still needed. In addition, our study indicates that parasite diversity in many regions is still under-explored, and thus we highlight the importance of studies of host-associated parasites, especially in the context of freshwater fish biogeography. Graphical Abstract

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