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. Graphical Abstract

Host-Specific Parasites Reveal the History and Biogeographical Contacts of Their Hosts: The Monogenea of Nearctic Cyprinoid Fishes

“…Genomic DNA was extracted separately from each parasite specimen (1–10 specimens per species) using the DNeasy Blood & Tissue Kit (Qiagen, Hilden, Germany) following the manufacturer’s protocol. Two fragments of nuclear ribosomal DNA, generally considered suitable markers for monogenean species determination and widely applied in phylogenetic studies of Dactylogyrus [ 10 , 12 , 13 , 14 , 15 , 18 , 25 ], were analyzed as follows: (i) a fragment spanning partial 18S rDNA and internal transcribed spacer (18S rDNA + ITS1); and (ii) a fragment of partial 28S rDNA.…”

“…The second dataset was based on concatenated data of partial 18S rDNA + ITS1 and 28S rDNA and included 36 sequences of North American Dactylogyrus species (all genetic variants for North American Dactylogyrus species exhibiting intraspecific variability were included) and the sequences of 17 selected Dactylogyrus species parasitizing European fishes of Leuciscidae and Cyprinidae [ 15 ]. Mid-point rooting was applied because of the ambiguous positions of lineages II and lineages III in relation to lineage IV revealed by previous phylogenetic studies [ 15 , 18 , 25 ]. Sequence divergence for the North American species exhibiting intraspecific variability between different localities was estimated in MEGA X [ 43 ] using the p-distance model.…”

“…Their study highlighted the role of continental bridges between southern Europe and North Africa playing a crucial role in the historical dispersion of cyprinids and also affecting the distribution of host-specific parasites of Dactylogyrus . Finally, Benovics et al [ 25 ] revealed that the Middle East represents the area of Dactylogyrus diversification and suggested that the attachment organ (termed the haptor) of each Dactylogyrus lineage has specific morphological characteristics that are associated with a particular dispersal event proposed for cyprinids.…”

Prevalence, molecular identification and host preference of Dactylogyrus, an ectoparasite in Indian major carps

“…The report on the prevalence of this particular parasite in aquaculture systems of India is scarce. Genus Dactylogurus has a high species diversity worldwide and the parasitic diversity in many regions is underexplored (Benovics et al, 2021). Hence, it is worth to explore species predominance in different aquaculture regions of the country.…”

First Study on Gyrodactylus (Monogenea: Gyrodactylidae) in Morocco, with Description of a New Species from Cyprinids (Actinopterygii: Cyprinidae)

“…From the three species of Gyrodactylus recorded from cyprinids in Africa, the here newly described species of Gyrodactylus can be differentiated by the longer hamuli: G. nyingiae n. sp. 76.5 (65.9-88.2) compared to a hamulus total length in G. ivindoensis of 55 (52-58), 32.1 (23)(24)(25)(26)(27)(28)(29)(30)(31)(32)(33) Due to the important biogeographical connections between the Middle East and Maghreb region during the Cenozoic period in the dispersal of freshwater fish fauna, it is interesting to compare the Gyrodactylus fauna of the Iranian region with the North African ones [3,30]. The freshwater species of Gyrodactylus mentioned by [31] and [32] (65.9-88.2).…”