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The Biology of Gyrodactylid Monogeneans: the ''Russian-Doll

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The Biology of Gyrodactylid Monogeneans: the ''Russian-Doll The Biology of Gyrodactylid Monogeneans: The ‘‘Russian-Doll Killers’’ T.A. Bakke1, J. Cable2 and P.D. Harris3,Ã 1Department of Zoology, Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, NO-0318 Oslo, Norway 2School of Biosciences, Cardiff University, Cardiff CF10 3TL, UK 3Schools of Education and Biology, University of Nottingham, Nottingham NG8 1BB, UK Abstract ...................................162 1. Introduction. ...............................164 1.1. Early History ........................... 165 1.2. Taxonomic and Faunistic Research ............. 166 1.3. The Gyrodactylus salaris Epidemic ............. 166 1.4. Genus, Species Flock or Host Races? . ........ 167 1.5. Gyrodactylus: The Drosophilids of the Parasitic World . 168 2. Morphology. ...............................169 2.1. The Importance of Progenesis and Viviparity ....... 170 2.2. Tegument . ............................ 174 2.3. Attachment and Musculature . ............... 175 2.4. Digestive System . ...................... 185 2.5. Glandular System . ...................... 189 2.6. Excretory System . ...................... 190 2.7. Nervous System . ...................... 190 2.8. Reproductive System ...................... 193 3. Ethology...................................201 3.1. General Behaviour. ...................... 201 3.2. Site Specificity and Migrations on the Host ........ 207 3.3. Migration Between Hosts: Lack of a Dispersive Phase . 214 4. Phylogeny: The Family Album . ..................217 4.1. Taxonomic History. ...................... 217 4.2. The Family Gyrodactylidae . ............... 220 4.3. The Genera ............................ 220 ÃThe authors contributed equally to this manuscript. ADVANCES IN PARASITOLOGY VOL 64 Copyright r 2007 Elsevier Ltd. ISSN: 0065-308X $35.00 All rights of reproduction in any form reserved DOI: 10.1016/S0065-308X(06)64003-7 162 T.A. BAKKE ET AL. 4.4. Evolutionary Affinities of the Gyrodactylids ........ 232 5. Systematics: The Biological Bedrock.................236 5.1. Morphological Conservatism . ............... 236 5.2. Molecular Genetics . ...................... 242 5.3. Host Specificity Among Gyrodactylids . ........ 251 6. Evolution and Phylogeny of Gyrodactylids . ...........259 6.1. Models of Parasite Speciation . ............... 259 6.2. Evolution of Gyrodactylids on Guppies . ........ 262 6.3. Species Flocks on Gobies................... 263 6.4. Refugia and Pleistocene Dispersals............. 266 6.5. Paraphyly of Gyrodactylus salaris .............. 271 6.6. Terminology of the G. salaris Species Complex . 278 7. Epidemiological Models: Bridging the Gap between Micro- and Macroparasites . .........................279 8. Host immunity and Parasite Pathogenicity . ...........280 8.1. Host Immune Responses ................... 280 8.2. The Heritability of Disease Resistance . ........ 288 8.3. Parasite Pathogenicity ..................... 290 8.4. Host Specificity and Immunity: Two Sides of the Same Coin? ................................ 293 9. Environmental Interactions .......................295 9.1. Micropredation .......................... 295 9.2. Temperature ........................... 296 9.3. Salinity and Water Chemistry . ............... 302 9.4. Pollution and Water Quality . ............... 305 10. The Gyrodactylus salaris Epidemic in Norway: Implications for other Countries . .........................306 10.1. History . ............................ 306 10.2. The Status of G. salaris within the EU . ........ 310 10.3. The Current Status of G. salaris in Norway ........ 314 10.4. Control Measures . ...................... 319 10.5. Potential for Further Spread of Gyrodactylus salaris . 326 11. Conclusions and Future Research Areas . ...........328 Acknowledgements. .........................330 References . ...............................330 ABSTRACT 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 THE BIOLOGY OF GYRODACTYLID MONOGENEANS 163 gyrodactylids from South American catfish, and highlight the plesiomor- phic characters shared by gyrodactylids and other primitive mono- geneans. 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 Polycli- thrinae should be allowed to lapse. We discuss approaches to the taxo- nomy 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 164 T.A. BAKKE ET AL. review the history and current status of the epidemic, and current strat- egies for elimination of the parasite from Norway. Finally, we consider opportunities for further spread of the parasite within and beyond Europe. 1. INTRODUCTION Monogeneans of the genus Gyrodactylus have been known for almost 180 years for their retention of fully grown daughters in utero until they themselves contain developing embryos (Figure 1). This ‘‘Rus- sian-doll’’ reproduction, dubbed hyperviviparity by Cohen (1977),is extremely rare in the Animal Kingdom and was the focus for inten- sive study by late 19th century microscopists. We recently reviewed gyrodactylid reproduction (Cable and Harris, 2002) and specificity (Bakke et al., 2002) but there are now compelling reasons to re- evaluate their ecology. In the first place, although the viviparous gyrodactylids have attracted most attention, we are becoming in- creasingly aware of the diversity of oviparous gyrodactylids from South American catfish (Kritsky et al., 2007) and a review of their relationship to the viviparous genera is timely. Furthermore, the vi- viparous gyrodactylids are increasingly reported as pathogens of Figure 1 Light micrograph (interference contrast) of a living gravid Gyrodactylus salaris with two daughters in utero like ‘‘a Russian-doll’’. The lack of penis and spermatozoa in the seminal receptacle together with the near term F1 embryo in utero indicates that the parasite has not yet given birth for the first time. (G. Robertsen, unpublished.) See coloured version on the front cover. THE BIOLOGY OF GYRODACTYLID MONOGENEANS 165 farmed fish (Lile et al., 1993; Woo, 1995; Mo and Lile, 1998; Jalali et al., 2005; You et al., 2006) and the notoriety of the Gyrodactylus salaris epidemic has stimulated research to such an extent that gyrodactylids are now the best studied of all monogeneans. Much research in Europe has focussed on three economically relevant species: G. salaris on Atlantic salmon (Salmo salar) and its non- pathogenic sibling G. thymalli on grayling (Thymallus thymallus), and G. derjavini on brown trout (Salmo trutta). Recent studies suggest that in the former case we are observing the evolution of a fish path- ogen complex in real time. However, several other gyrodactylids have also been studied extensively, including those infecting guppies, gobies and sticklebacks, and represent ideal model systems for study- ing evolutionary and ecological processes in this group, and in para- sitic organisms in general. 1.1. Early History Gyrodactylus was first described from bream (Abramis brama)by von Nordmann (1832). Although he observed the embryo in utero, he failed to appreciate its significance, and the prominent embryonic hamuli (Figure 1) were interpreted
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