Hybrid origin of Baltic salmon‐specific parasite Gyrodactylus salaris: a model for speciation by host switch for hemiclonal organisms

Abstract

Host switching explains the high species number of ectoparasitic, viviparous, mainly parthenogenetic but potentially hermaphroditic flatworms of the genus Gyrodactylus. The starlike mitochondrial phylogeny of Gyrodactylus salaris suggested parallel divergence of several clades on grayling (also named as Gyrodactylus thymalli) and an embedded sister clade on Baltic salmon. The hypothesis that the parasite switched from grayling to salmon during the glacial diaspora was tested using a 493-bp nuclear DNA marker ADNAM1. The parasites on salmon in lakes Onega and Ladoga were heterozygous for divergent ADNAM1 alleles WS1 and BS1, found as nearly fixed in grayling parasites in the White Sea and Baltic Sea basins, respectively. In the Baltic salmon-specific mtDNA clade, the WS/BS heterozygosity was maintained in 23 out of the 24 local clones. The permanently heterozygous clade was endemic in the Baltic Sea basin, and it had accumulated variation in mtDNA (31 variable sites on 1600 bp) and in the alleles of the nuclear locus (two point mutations and three nucleotide conversions along 493 bp). Mendelian shuffling of the nuclear alleles between the local clones indicated rare sex within the clade, but the WS/BS heterozygosity was lost in only one salmon hatchery clone, which was heterozygous WS1/WS3. The Baltic salmon-specific G. salaris lineage was monophyletic, descending from a single historical hybridization and consequential host switch, frozen by permanent heterozygosity. A possible time for the hybridization of grayling parasite strains from the White Sea and Baltic Sea basins was during the Eemian interglacial 132 000 years bp. Strains having a separate divergent mtDNA observed on farmed rainbow trout, and on salmon in Russian lake Kuito were suggested to be clones derived from secondary and tertiary recombination events.

Description of three new European cryptic species of Gyrodactylus Nordmann, 1832 supported by nuclear and mitochondrial phylogenetic characterization

“…If the mtDNA sequence of some considerable length of two specimens is identical, then their most recent maternal ancestor existed quite recently. The divergence rate of mtDNA in G. salaris was estimated to be 7.6 to 13.3% per million years (Kuusela et al 2007). For mtDNA, the tolerance to accept two sequences to be similar enough to belong to the same species should be higher than for ITS, but perhaps less than ten percent.…”

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

“…If it is justly assumed that distant hybridization is rare, this Polish-Macedonian divergence in the mitochondrial sequence suggests that the alien mtDNA was introduced into the G. salaris genome once, but a long time ago. A divergence rate of up to 13% per million years has been suggested for this segment of mtDNA in G. salaris (Kuusela et al 2007). Using this value, the hybridization occurred about one hundred thousand years ago (137-57 kyr).…”

“…However, the mitochondrial marker alone is not enough for a detailed evolutionary analysis of the aspects of host specificity and pathogenity, as discussed in the comprehensive review by Hansen et al (2007b). The hybrid origin of the main mtDNA clade parasitizing Baltic salmon was solved by adding a variable nuclear DNA marker to the toolbox (Kuusela et al 2007). The mitochondrially separate clade associated in several localities with rainbow trout, Arctic charr, and salmon, and specified as the RBT clone by Zię-tara et al (2006), or clade F by Hansen et al (2007b), remains of unknown origin.…”

High Gyrodactylus salaris infection rate in triploid Atlantic salmon Salmo salar

“…Importantly, Atlantic salmon populations exhibit marked differences in susceptibility to G. salaris infection, with populations from the Atlantic and the White Sea coasts exhibiting higher infection rates and increased mortality, while salmon populations from the Baltic basin are more resistant to the parasite (Bakke et al 1992, Rintamäki-Kinnunen & Valtonen 1996, Dalgaard et al 2003, Kuusela et al 2009). The most severe G. salaris outbreaks have been observed in Norway, where epidemics of this parasite have devastated salmon stocks > 46 rivers over the last 25 yr (Johnsen & Jensen 1991, Johnsen et al 1999, Kuusela et al 2007, Buchmann 2008. Despite the fact that Baltic salmon are generally believed to be more resistant to G. salaris, the susceptibility level varies among populations.…”

“…parasites collected from 2 different hosts were sequenced for the ITS; 3 parasites collected from 3 different hosts were sequenced for mtDNA CO1; and 9 parasites collected from 5 hosts were sequenced for nuclear anonymous DNA marker (ADNAM1). In addition, 32 parasites collected from 8 salmon were screened for ADNAM1 using agarose gel electrophoresis (Ziętara et al 2006).The mitochondrial and variable nuclear marker sequences were compared with earlier published Gyrodactylus salaris CO1 and ADNAM1 sequences (Kuusela et al 2007(Kuusela et al , 2009). For clarification of isolated parasite strain genetic relationships with other strains, a Neighbor-joining tree (NJ tree) based on mtDNA CO1 sequence using maximum composite likelihood distance was constructed, with 1000 bootstrap replicates.…”