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

Michal Benovics,Farshad Nejat,Andrea Šimková,Asghar Abdoli

doi:10.1186/s13071-021-04863-7

Michal Benovics, Farshad Nejat + Show 2 more

Open Access

https://doi.org/10.1186/s13071-021-04863-7

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Abstract

BackgroundFreshwater 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.MethodsA 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.ResultsThe 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.ConclusionsThe 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

Highlights

Freshwater fauna of the Middle East encompass elements shared with three continents—Africa, Asia, and Europe—and the Middle East is, considered a historical geographic crossroad between these three regions
Our study indicates that parasite diversity in many regions is still under-explored, and we highlight the importance of studies of host-associated parasites, especially in the context of freshwater fish biogeography
Haptor morphometrics and the presence of specific sclerites apparently play an important role in the host specificity of Dactylogyrus, as the parasites of this genus require a high level of adaptation for the specific microhabitats provided by hosts ([12,13,14], reviewed in [10])

Summary

Introduction

Freshwater fauna of the Middle East encompass elements shared with three continents—Africa, Asia, and Europe—and the Middle East is, considered a historical geographic crossroad between these three regions. We investigated the proposed scenarios using monogenean parasites of the genus Dactylogyrus, which is host-specific to cyprinoid fishes. One of the most important events in the evolutionary history of parasites is cospeciation with their hosts, leading to the emergence of new species of parasites during the speciation of their hosts, which often occurs in allopatry [1]. Some generalist species (e.g., D. sphyrna, D. vastator, and D. vistulae) have not developed a haptoral ventral connective bar. As this morphological feature is present in Dactylogyrus species of different phylogenetic lineages, it was hypothesized by Benovics et al [15] that the secondary loss of the ventral connective bar may allow the parasite to infect a wider range of hosts. Šimková et al [16] hypothesized that attachment organs with large-sized anchoral sclerites promote the colonization of several phylogenetically distant host species

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