The phylogeography of salmonid proliferative kidney disease in Europe and North America

Abstract

Salmonid proliferative kidney disease (PKD) is caused by the myxozoan Tetracapsuloides bryosalmonae. Given the serious and apparently growing impact of PKD on farmed and wild salmonids, we undertook a phylogeographic study to gain insights into the history of genealogical lineages of T. bryosalmonae in Europe and North America, and to determine if the global expansion of rainbow trout farming has spread the disease. Phylogenetic analyses of internal transcribed spacer 1 sequences revealed a clade composed of all North American sequences plus a subset of Italian and French sequences. High genetic diversity in North America and the absence of genotypes diagnostic of the North American clade in the rest of Europe imply that southern Europe was colonized by immigration from North America; however, sequence divergence suggests that this colonization substantially pre-dated fisheries activities. Furthermore, the lack of southern European lineages in the rest of Europe, despite widespread rainbow trout farming, indicates that T. bryosalmonae is not transported through fisheries activities. This result strikingly contrasts with the commonness of fisheries-related introductions of other pathogens and parasites and indicates that fishes may be dead-end hosts. Our results also demonstrate that European strains of T. bryosalmonae infect and induce PKD in rainbow trout introduced to Europe.

Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea), the causative organism of salmonid proliferative kidney disease, to the freshwater bryozoan Fredericella sultana

“…This led to the suggestion that there is a European strain of the parasite and a North American one, adapted to species of Salmo and Oncorhynchus respectively (Bucke et al 1991 ;Morris et al 1997). Distinct genetic differences have been found to exist between T. bryosalmonae isolates obtained from the two continents (Henderson and Okamura, 2004) and this further supports the hypothesis of T. bryosalmonae strains adapted to indigenous salmonids. It is important that the ability of a range of salmonids to transmit the infection to bryozoans is further examined; both to verify the results of the brown trout transmission experiment and to determine precisely which species are involved in the life-cycle of this parasite.…”

“…The stocking of infected fish has been suggested as a mechanism to account for the spread of PKD in Swiss brown trout populations (Wahli et al 2002). The original intercontinental translocation of the parasite pre-dates fisheries activities (Henderson and Okamura, 2004) and may have occurred through species of susceptible bryozoans and salmonids such as Artic charr that have natural distributions spanning the northern hemisphere. The remarkable ecological plasticity of some salmonids such as brown trout would further facilitate the distribution of the parasite to a diverse range of habitats while intra-clonal propagation through fragmentation of bryozoan colonies may assist the establishment of the parasite into new water bodies by increasing the spread of infected bryozoans within a body.…”

Tetracapsuloides bryosalmonae and PKD in juvenile wild salmonids in Denmark

“…the Jutland peninsula and the islands of Sealand and Funen) tended to cluster separately in the phylogenetic analysis. Such a biogeographic pattern is not the general picture for this parasite (Henderson & Okamura 2004). On the contrary, identical ITS phylotypes usually occur in host species from far separate geographic localities.…”

Early development of the myxozoan Buddenbrockia plumatellae in the bryozoans Hyalinella punctata and Plumatella fungosa, with comments on taxonomy and systematics of the Myxozoa

“…Since the recognition of the Malacosporea in 2000 (Canning et al 2000), evidence for four species (including "T. bryozoides") has been gathered (Tops et al 2005) and the spatial scale of sampling populations has expanded greatly (e.g. Okamura et al 2001, Henderson and Okamura 2004. We can expect that future studies will improve our understanding of malacosporean diversity and taxonomy.…”