The phylogenetic relationships and species richness of host-specific Dactylogyrus parasites shaped by the biogeography of Balkan cyprinids

Michal Benovics,Yves Desdevises,Jasna Vukić,Andrea Šimková,Radek Šanda

doi:10.1038/s41598-018-31382-w

Abstract

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.

Highlights

The species richness of parasitic taxa and their distribution in host species is usually closely related to the history, dispersion and diversity of their hosts[1,2,3]
The highest Dactylogyrus species diversity was reported on representatives of the genera Pachychilon – P. pictum (5); Squalius – S. squalus (4) and S. prespensis (4); Barbus – B. prespensis (4); and Rutilus – R. basak (4), R. lacustris (4), and R. ohridanus (4)
We observed a maximum of 5 Dactylogyrus species on a single cyprinid species

Summary

Introduction

The species richness of parasitic taxa and their distribution in host species is usually closely related to the history, dispersion and diversity of their hosts[1,2,3]. The second period is related to the Plio-Pleistocene connection of the Balkan Peninsula and the River Danube via river captures[23,24] This dispersion event included species such are Barbus balcanicus[25], Squalius vardarensis and species of Chondrostoma and Alburnus genera[26], which exhibit a much lower degree of molecular divergence with respect to Danubian-related taxa. A phylogenetic reconstruction including 51 Dactylogyrus species and based on molecular data suggested that species parasitizing central European cyprinids form three monophyletic groups[11] and are associated with different phylogenetic lineages of cyprinid species representing subfamilies with different origins, histories, and biogeographical distributions. Dupont[44] investigated the historical biogeography of Dactylogyrus species of endemic Rutilus, Luciobarbus, and Pachychilon hosts from the Balkan Peninsula and suggested that the endemism of Dactylogyrus can be explained by the formation of landmass and freshwater streams during the Neogene and Pleistocene eras

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