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Molecular and morphological phylogeny of host-specific Dactylogyrus parasites (Monogenea) sheds new light on the puzzling Middle Eastern origin of European and African lineages.

ABSTRACT:

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.

SUBMITTER: Benovics M

PROVIDER: S-EPMC8293574 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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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