The phylogenetic position of the enigmatic Balkan Aulopyge huegelii (Teleostei: Cyprinidae) from the perspective of host-specific Dactylogyrus parasites (Monogenea), with a description of Dactylogyrus omenti n. sp.

Abstract

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.

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

“…The phylogenetic position of D. omenti among Dactylogyrus species parasitizing Barbus and Luciobarbus was already suggested by Benovics et al . 65 . Even though its exact phylogenetic position is not fully resolved, our result suggests that this species is phylogenetically closer to D. petenyi and D. prespensis than to the aforementioned species which share the ‘cornu’ type of haptoral ventral bar.…”

Cophylogenetic relationships betweenDactylogyrus(Monogenea) ectoparasites and endemic cyprinoids of the north‐eastern European peri‐Mediterranean region

“…cophylogeny, Cyprinoidea, Monogenea, phylogeny Several coevolutionary scenarios were proposed by Benovics et al (2017), Benovics, Desdevises, Vukić, Šanda, and Šimková (2018), and Šimková, Benovics, Rahmouni, and Vukić (2017) regarding Dactylogyrus and peri-Mediterranean endemic cyprinoids, the last one hypothesizing that Iberian cyprinids harbour Dactylogyrus species originating from two different colonization events.…”

“…However, many of the northern and north-eastern Mediterranean drainages are heavily affected by introductions of non-native freshwater species, including numerous cyprinoids (Bianco, 1995;Piria et al, 2018;Vukić, Eliášová, Marić, & Šanda, 2019), even the endemic ones being translocated often outside the native range (Bianco, 1995;Koutsikos et al, 2019). This could lead to the simultaneous introduction of their non-native parasite species, which can subsequently infect the native fishes (such as parasite Dactylogyrus, documented in Benovics et al, 2017).…”

“…Dactylogyrus Diesing, 1850 (Monogenea) are gill parasites generally exhibiting narrow host specificity and high morphological variability with respect to attachment organ (termed haptor), putatively reflecting adaptations to their different host species or within‐host microhabitats (Gibson, Timofeeva, & Gerasev, ; Šimková, Desdevises, Gelnar, & Morand, , ; Šimková & Morand, ; Šimková, Verneau, Gelnar, & Morand, ). In addition, Dactylogyrus currently represents the platyhelminth genus with the highest species diversity (more than 900 described species according to Gibson et al, ), certainly largely underestimated as new species have recently been described (Aydogdu, Molnár, Emre, & Emre, ; Benovics, Kičinjaová, & Šimková, ; Nitta & Nagasawa, ; Rahmouni, Řehulková, Pariselle, Rkhami, & Šimková, ). This high species richness in Dactylogyrus is associated with their narrow host specificity towards a single host species or closely related species, and with a high diversity of their host species—primarily freshwater fish of Cyprinoidea (considering recent phylogenetic studies, for example Schönhuth, Vukić, Šanda, Yang, & Mayden, ).…”

Uncovering the diversity of monogeneans (Platyhelminthes) on endemic cypriniform fishes of the Balkan Peninsula: new species of Dactylogyrus and comments on their phylogeny and host-parasite associations in a biogeographic context

“…To date, only a limited number of studies have been focused on investigating the diversity and/or phylogenetic relationships of Dactylogyrus spp. parasitizing the Balkan cypriniform fishes [3,4,18,19,71,[81][82][83][84]. Recently, Benovics et al [4] revealed eight potentially new Dactylogyrus species on two species of cyprinids (Luciobarbus albanicus and L. graecus) and six species of leuciscids (Chondrostoma knerii Heckel, Delminichthys adspersus (Heckel), Pachychilon macedonicum (Steindachner), Squalius tenellus Heckel, Tropidophoxinellus spartiaticus (Schmidt-Ries), and Telestes karsticus Marčić & Mrakovčić).…”