Ectoparasitism in Polystomatidae (Neodermata, Monogenea): phylogenetic position and mitogenome of Sphyranura euryceae, a parasite of the Oklahoma salamander

Abstract

BackgroundPolystomatidae represents a monogenean group whose representatives infect mainly (semi)-aquatic tetrapods. Sphyranuridae with its single genus (Sphyranura) exhibits ectoparasitism on salamander hosts and was traditionally considered a sister-group to Polystomatidae based on the presence of a well-developed opisthaptor yet was distinguished due to the presence of a single pair of haptoral suckers, as opposed to the three pairs present in polystomatids. However, more recent molecular work supported its inclusion within Polystomatidae, at an early diverging, yet unresolved, position in the clade of polystomatids that otherwise exhibit endoparasitism of batrachians. Resolving the position of Sphyranura in relation to Polystomatidae is a prerequisite for understanding the factors driving evolution and the shifts between ecto- and endoparasitism in Polystomatidae. MethodsVarious staining methods were used to morphologically characterise collected specimens of Sphyranura. The mitochondrial genome was assembled from WGS data. Based on a combination of nuclear (18S, 28S rRNA) and mitochondrial markers (cox1, 12S) we inferred the phylogeny of Polystomatidae using Bayesian inference and maximum likelihood methods. ResultsBased on morphological examination and comparison with type material, specimens of Sphyranura infecting Oklahoma salamander (Eurycea tynerensis) at Greathouse Spring, Arkansas (USA), were identified as S. euryceae, a new distributional record for the species. Along with an amended diagnosis of Sphyranura we provide the first molecular data for S. euryceae. Mitochondrial level comparison reveals instances of tRNA gene rearrangements in polystomatids. Our phylogeny identifies two clades within polystomatids infecting tetrapods, one infecting exclusively batrachians, the other mainly known from chelonians. Although not fully supported, Sphyranura appears as the earliest branching lineage within the former. ConclusionsWith Sphyranura nested within Polystomatidae, we consider Sphyranuridae invalid. Sphyranuras apparent early branching position indicates ectoparasitism is an ancestral trait with endoparasitism having evolved later in the Polbatrach clade. However, the reduced number of haptoral suckers in representatives of Sphyranura is a derived characteristic potentially resulting from paedomorphic evolution. Whilst there is an indication towards phylogenetic congruence of polystomatids and their batrachian hosts, the same was not true for polystomatid parasites of chelonians with evidence of multiple host switches. Furthermore, geographic distribution of hosts was not found to drive polystomatid phylogeny.