Global Phylogeography of Salmonid Ectoparasites of the Genus Gyrodactylus, with an Emphasis on the Origin of the Circumpolar Gyrodactylus salmonis (Platyhelminthes: Monogenea)

ABSTRACT: The wageneri species group of Gyrodactylus contains the following molecularly confirmed salmonid parasites in Asia: Gyrodactylus taimeni Ergens, 1971, Gyrodactylus magnus Konovalov, 1967, Gyrodactylus brachymystacis Ergens, 1978, and Gyrodactylus derjavini Mikhailov, 1975; in Europe it contains the following: Gyrodactylus derjavinoides Malmberg, Collins, Cunningham, and Jalali, 2007, Gyrodactylus truttae Gläser, 1974, Gyrodactylus teuchis Lautraite, Blanc, Thiery, Daniel, and Vigneulle, 1999, Gyrodactylus lavareti Malmberg, 1956, Gyrodactylus salvelini Kuusela, Ziętara, and Lumme, 2008 (presented herein as a junior synonym of Gyrodactylus salmonis Yin and Sproston, 1948), and Gyrodactylus salaris Malmberg, 1957, with the lone confirmed North American exception being G. salmonis. The mitochondrial DNA (cox1, 1545 bp) of this group shows a star-like phylogenetic expansion that began 2.05 ± 0.4 million years ago (mya), estimated from the mean distance of the cox1 gene (dMCL = 0.267) using a tentative, potentially high-end, divergence rate of 0.13/Myr. European G. salaris on Thymallus thymallus and Asian G. magnus on Thymallus arcticus have been separated for 1.95 Myr (dMCL = 0.253). The nuclear ITS rDNA region (1,245 bp) of G. salmonis was nearly uniform among North American populations of Oncorhynchus mykiss, Oncorhynchus clarkii, Oncorhynchus nerka, Salvelinus fontinalis, and Salmo salar (and non-native Salmo trutta) as well as on Salvelinus alpinus (under the synonym G. salvelini) from Lake Inari, Finland. Gyrodactylus salmonis is distal in a monophyletic subclade labeled by an apomorphic 56 bp insertion in the ITS1, shared by the European parasites G. lavareti (host: Coregonus lavaretus), Gyrodactylus pomeraniae Kuusela, Ziętara, and Lumme, 2008 (host: Rutilus rutilus), and Gyrodactylus bliccensis Gläser, 1974 (host: Alburnus alburnus). This subphylogeny suggests that a particular host switch from cyprinids to salmonids may have occurred less than 1.8 mya in the Old World [dMCL = 0.234 G. pomeraniae vs (G. salmonis, G. lavareti)] and possibly again among coregonine hosts and Salvelinus 1.2 mya (dMCL = 0.156). Although hypothetical, a transition from coregonines to charr (notably the widely distributed and adaptable Salvelinus alpinus) potentially could have occurred in a proglacial refugium leading to circumpolar distribution of G. salmonis and a secondary transition to other North American hosts. The maximum cox1 genetic distance within G. salmonis on all hosts was dMCL = 0.032, at the same level as in multihosted European G. salaris (dMCL = 0.032), suggesting circa 250,000 yr of population expansion with these parasites since a temporal, coinciding bottleneck.