Host switching via rare sex: Oncorhynchus mykiss as a vector in fusion of three Gyrodactylus salaris genomes into a sexual-clonal population on a landlocked Salmo salar (Monogenea, Platyhelminthes).

The monogenean ectoparasite Gyrodactylus salaris Malmberg, 1957 was detected in 2001 on juveniles of landlocked Salmo salar Linnaeus in three rivers draining to Lake Kuitozero in the White Sea basin. The ancestry of the colony was studied by internal transcribed spacers of the nuclear ribosomal operon (ITS), mitochondrial COI gene and by 12 microsatellite markers. The maternal ancestor was a frozen heterozygotic and heteroplasmic diploid clone RBT marked by a ITS-1068R, spread by rainbow trout and observed in Denmark, Norway, Finland and Russia. The clone combined genomes from two divergent matrilines, probably from grayling (Thymallus Linck) in the Southern Baltic basin (COI alien, 84 % bootstrap support) and in Balkans (COI rbt, 99 %). The genetic distance of the 1545 bp sequences was dMCL = 0.025. The population in Kuitozero was a progeny of RBT females repeatedly inseminated by conspecific males. It was sexual but propagated as parthenogenetic clones. The derived population carried only COI rbt.. The microsatellite alleles of the RBT clone segregated with the paternal alleles following Mendelian model, with an excess of heterozygotes: He = 0.608, Ho = 0.883. Among 244 genotyped worms, 27 multilocus clones were observed, as segregated among the parr (FST = 0.824). Parental genotypes were not detected. The largest clone (104 worms) was heterozygotic in all 12 loci and was identified on fifteen fish, in two rivers and four years. The balancing selection (excess of heterozygotes) equalised the allelic frequencies and maximised the genetic variance available for purifying and adaptive natural selection on a new host. The two sexual episodes associated with three host switch steps offers a model to understand the evolution of the diverse host spectrum of host-specific Gyrodactylus von Nordmann, 1832.