The incongruence of nuclear and mitochondrial DNA variation supports conspecificity of the monogenean parasites Gyrodactylus salaris and G. thymalli

Abstract

The monogenean Gyrodactylus salaris Malmberg, 1957 is an economically important parasite on Atlantic salmon whereas the morphologically very similar G. thymalli Zitnan, 1960 on grayling is considered harmless. Even molecular markers cannot unambiguously discriminate both species. The nuclear internal transcribed spacer (ITS) sequences are identical in both species, and although mitochondrial cytochrome oxidase I (COI) sequences show substantial variation, no support for monophyly of either species is found. Analysis of nucleotide sequences of the intergenic spacer (IGS) have, however, been interpreted as support for 2 species. Here, IGS and COI sequences from 81 G. salaris and G. thymalli specimens of 39 populations across the species' distribution range were determined. Mitochondrial diversity was not reflected in the nuclear marker. Since various 23 bp IGS repeat types usually differ by just one nucleotide and sequences primarily differ in the number and order of repeat types, alignments may be biased and arbitrary, impeding meaningful phylogenetic analyses. The hypothesis that parasites on rainbow trout represent hybrids of both species is rejected. The presence or absence of particular repeat types is not considered informative. We interpret the IGS data as support for G. salaris and G. thymalli being a single species.

The first report of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes, Monogenea) on Italian cultured stocks of rainbow trout (Oncorhynchus mykiss Walbaum)

“…Identification of most of the G. salaris specimens as haplotype F (Table 1), which are common in rainbow trout farms, provides supporting evidence to suggest that G. salaris has mainly been spread via the rainbow trout trade rather than from the local indigenous fish population. The finding of a new haplotype on rainbow trout is not surprising as several haplotypes have been recovered from salmon and grayling (Hansen et al, 2003(Hansen et al, , 2006Meinilä et al, 2004). Further investigation, however, is needed to ascertain whether this infection originates from rainbow trout introduced to the farm or from wild fish in the River Nera.…”

“…For the seven specimens identified as G. salaris by morphological analysis or by sequencing of ITS, the base sequence of their cytochrome oxidase I genes were also determined. Six of the sequences corresponded to the mitochondrial F haplotype that is common in rainbow trout farms across Europe (see Meinilä et al, 2004;Hansen et al, 2003Hansen et al, , 2006Hansen et al, , 2007 and three of these sequences contained some ambiguities that could be the result of PCR or sequencing errors. The last sequence represents a new haplotype of G. salaris and is submitted under GenBank accession number GQ370816.…”

“…The discrimination of G. salaris from other related species is, however, not always straightforward. Gyrodactylus salaris and the purported non-pathogenic Gyrodactylus thymalli Žitň an, 1960 from grayling, Thymallus thymallus L., are morphologically similar, their ITS sequences are practically identical, and recent studies indicate that the two species might be conspecific (Zię tara and Lumme, 2002;Hansen et al, 2003Hansen et al, , 2006Hansen et al, , 2007Meinilä et al, 2004). Analyses of the mitochondrial cytochrome oxidase I gene (COI), however, show that G. salaris and G. thymalli can be grouped in different clades and that all the gyrodactylids from rainbow trout appear to belong to the same COI haplotype (Hansen et al, 2003;Meinilä et al, 2004).…”

Introgression of distant mitochondria into the genome of Gyrodactylus salaris: Nuclear and mitochondrial markers are necessary to identify parasite strains

“…Sequencing of the mitochondrial DNA (mtDNA) has revealed an unexpected scale of diversity and geographical structure in the natural Baltic range on Atlantic salmon, Salmo salar L. ), as well as on different host species like rainbow trout, Oncorhynchus mykiss (W.) and Arctic charr, Salvelinus alpinus (L.) (Meinilä et al 2002(Meinilä et al , 2004Hansen et al 2003Hansen et al , 2006Hansen et al , 2007aRobertsen et al 2007). The mtDNA offers high resolution for separating numerous host-specific and geographically separated strains of salmon parasites and those on grayling, Thymallus thymallus (L.) (which are also called G. thymalli Žitňan).…”

Identification of Gyrodactylus ectoparasites in Polish salmonid farms by PCR-RFLP of the nuclear ITS segment of ribosomal DNA (Monogenea, Gyrodactylidae)

“…At present, the internal transcribed spacers (ITS1 and ITS2) of nuclear ribosomal RNA genes are the most common molecular marker used to discriminate these parasites (Cunningham 1997;Matìjusová et al 2001Matìjusová et al , 2003Ziêtara et al 2000;Ziêtara and Lumme 2004). The intergenic spacer (IGS) of ribosomal RNA genes have also been tested for G. salaris and G. thymalli , Sterud et al 2002, Hansen et al 2006. The subunit 1 of the mitochondrial cytochrome oxidase (COI) gene may also be used successfully to differentiate species and local Gyrodactylus strains (Meinilä et al 2002(Meinilä et al , 2004Hansen et al 2003Hansen et al , 2007.…”