Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae)

Abstract

To test the hypothesis that host-switching can be an important step in the speciation of gyrodactylid monogenean flatworms, we inferred the phylogeny within a cluster of parasites morphologically close to Gyrodactylus salaris Malmberg 1957, collected from Atlantic, Baltic and White Sea salmon ( Salmo salar), farmed rainbow trout ( Oncorhynchus mykiss), and grayling ( Thymallus thymallus) from Northern Europe. The internal transcribed spacer region of the nuclear ribosomal gene was sequenced for taxonomic identification. Parasites on grayling from the White Sea Basin differed from the others by one nucleotide (0.08%), the remainder were identical to the sequence published earlier from Norway ( G. salaris on salmon), England ( Gyrodactylus thymalli on grayling), and the Czech Republic (unidentified salaris/thymalli on trout). For increased resolution, 813 nucleotides of the mitochondrial COI gene of 88 parasites were sequenced and compared with 76 published sequences using phylogenetic analysis. For all tree building algorithms (NJ, MP), the parasites formed a star-like phylogeny of six definite sister clades, indicating nearly simultaneous radiation. Average K2P distances between clades were 1.8–2.6%, and internal mean distances 0.2–1.1%. The genetic distance to the nearest known relative, Gyrodactylus lavareti Malmberg, was 24%. A variable salmon-specific mitochondrial Clade I was observed both in the Baltic Basin and in pathogenic populations introduced to the Atlantic and White Sea coasts. An invariable Clade II was common in rainbow trout farms in Sweden, Denmark and Finland; the same haplotype was also infecting salmon in a landlocked population in Russian Karelia, and in Oslo fjord and Sognefjord in Norway. Four geographically vicariant sister clades were observed on graylings: Clade III in the Baltic Sea Basin; Clade IV in Karelian rivers draining to the White Sea; Clade V in Norwegian river draining to Swedish lake Vänern; and Clade VI in rivers draining to Oslo fjord. The pattern fitted perfectly with the postglacial history of grayling distribution. Widely sampled clades from salmon and Baltic grayling had basal haplotypes in populations, which were isolated early during the postglacial recolonisation. The divergence between the six clades was clear and linked with their hosts, but not wide enough to support a species status for them. Parasites from the Slovakian type population of G. thymalli were not available, so this result does not mean that G. salaris and G. thymalli are synonyms. It is suggested that the plesiomorphic host of the parasite cluster was grayling, and the switch to salmon occurred at least once when the continental ice isolated Baltic salmon in an eastern freshwater refugium, 130,000 years ago. At the same time, parasites on grayling were split geographically and isolated into several allopatric refugia. The divergence among the parasite clades allowed a tentative calibration of the evolutionary rate, leading to an estimate of the divergence of 13.7–20.3% per million years for COI coding mtDNA. The results supported the hypothesis that parallel to the allopatric mode, host switch and instant isolation by host specificity can be operated as a speciation mechanism.