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The biology of gyrodactylid monogeneans: the "Russian-doll killers".

This article reviews the history of gyrodactylid research focussing on the unique anatomy, behaviour, ecology and evolution of the viviparous forms while identifying gaps in our knowledge and directions for future research. We provide the first summary of research on the oviparous gyrodactylids from South American catfish, and highlight the plesiomorphic characters shared by gyrodactylids and other primitive monogeneans. Of these, the most important are the crawling, unciliated larva and the spike sensilla of the cephalic lobes. These characters allow gyrodactylids to transfer between hosts at any stage of the life cycle, without a specific transmission stage. We emphasise the importance of progenesis in shaping the evolution of the viviparous genera and discuss the relative extent of progenesis in the different genera. The validity of the familial classification is discussed and we conclude that the most significant division within the family is between the oviparous and the viviparous genera. The older divisions into Isancistrinae and Polyclithrinae should be allowed to lapse. We discuss approaches to the taxonomy of gyrodactylids, and we emphasise the importance of adequate morphological and molecular data in new descriptions. Host specificity patterns in gyrodactylids are discussed extensively and we note the importance of host shifts, revealed by molecular data, in the evolution of gyrodactylids. To date, the most closely related gyrodactylids have not been found on closely related hosts, demonstrating the importance of host shifts in their evolution. The most closely related species pair is that of G. salaris and G. thymalli, and we provide an account of the patterns of evolution taking place in different mitochondrial clades of this species complex. The host specificity of these clades is reviewed, demonstrating that, although each clade has its preferred host, there is a range of specificity to different salmonids, providing opportunities for complex patterns of survival and interbreeding in Scandinavia. At the same time, we identify trends in systematics and phylogeny relevant to the G. salaris epidemics on Atlantic salmon in Norway, which can be applied more generally to parasite epidemiology and evolution. Although much of gyrodactylid research in the last 30 years has been directed towards salmonid parasites, there is great potential in using other experimental systems, such as the gyrodactylids of poeciliids and sticklebacks. We also highlight the role of glacial lakes and modified river systems during the ice ages in gyrodactylid speciation, and suggest that salmon infecting clades of G. salaris first arose from G. thymalli in such lakes, but failed to spread fully across Scandinavia before further dispersal was ended by rising sea levels. This dispersal has been continued by human activity, leading to the appearance of G. salaris as a pathogen in Norway. We review the history and current status of the epidemic, and current strategies for elimination of the parasite from Norway. Finally, we consider opportunities for further spread of the parasite within and beyond Europe.

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