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Evolution and phylogeography of salmonids and Gyrodactylus in Fennoscandia

A video: Gyrodactylus arcuatus happily playing on fin of Gasterosteus aculeatus:

arcuatus 005 (2).avi

Jaakko Lumme

Heidi Aisala

Julia Barskaya

Darya Lebedeva

Marek Zietara  Copacabana


Mikhail OzerovAlexey VeselovCraig Primmer Anni Tonteri

Salmon populations and Gyrodactylus parasite in the great lakes in Russian Karelia 

Project 2008-2010 supported by Finnish Academy (Collaboration with Craig Primmer, University of Turku, and Alexey Veselov, Karelian Research Center, Petrozavodsk):

We  have studied the population structure of salmon (Salmo salar) and other salmonids in Eastern Fennoscandia since 1999. In the latest project, the focus was/is in the great lakes Onega (Ääninen) and Ladoga (Laatokka). The genetic variation, temporal stability and divergence of six salmon spawning rivers in both lakes has been investigated. The endemic parasite Gyrodactylus salaris is very rare in these lakes, but there are reasons to believe that the parasite switched just to these populations less than 130 000 years ago, after the Eemian interglacial. That's why these populations are very resistant against the parasite, which is fatal for salmon populations in the White Sea and Atlantic coast. The genetic basis of the resistance is under study.

A recent phenomenon in the large lakes is the rainbow trout farming industry. With the juveniles transported from Finland, the rainbow trout specific Gyrodactylus salaris has been introduced, and we can only monitor the salmon rivers, to see if the parasites hybridize with endemic clones (on salmon and grayling) to produce new "superparasites", a model sadly known from Norway.

Genomic analysis of host specificity of Gyrodactylus salaris, a monogenean ectoparasite of fish

Project supported by Finnish Academy 2010-2013 and continued

We aim to genetically dissect the host specificity of divergent strains (clones) of Gyrodactylus salaris by 454 sequencing and bioinformatics. The olfactory and gustatory receptors will be identified by their structural characteristics, and the polymorphism of the receptors among the phenotypically divergent clones is then utilized to predict the functional genotype responsible for the specificity of the parasites on Atlantic salmon (Salmo salar), rainbow trout (Oncorhynchus mykiss), and grayling (Thymallus thymallus). March 2010, the assembly contains 61 Mb. The estimated genome of Gyrodactylus salaris is <100 Mb.

Global systematics of Gyrodactylus

Project continued since 1999, as a hobby

To obtain background information and to understand the evolution of Gyrodactylus in the global context, we are interested in the molecular systematics of the genus, which may contain 100 000 species on marine and freshwater fishes all round the globe. The genus is too large to manage, and it should be split to many genera. The molecular identification by ITS of rDNA helps in bookkeeping, while the traditional moprhological systematics is running to the bitter end. This project is run more like a hobby, and it depends on availability of samples from different parts of the world (E.g., Rokicka et al. 2009, Ziętara et al.2012, Lumme et al. 2016b, 2017; Reyda et al., 2019). Full coverage is not expected. 



Reyda, F.B., Wells, S.M., Ermolenko, A. V. , Ziętara, M.S., Lumme, J. (in press 2019) Global parasite trafficking: Asian Gyrodactylus (Monogenea) arrived to the U.S.A. via invasive fish Misgurnus anguillicaudatus as a threat to amphibians. Biological Invasions (accepted Sept. 11, 2019)

Zueva, K.J., Lumme, J., Veselov, A.E., Kent, M.P., Primmer, C.R. (2018) Genomic signatures of parasite-driven natural selection in north European Atlantic salmon (Salmo salar). Marine Genomics Volume 39, June 2018, Pages 26-38 (online 10 April 2018)

Lumme, J., Ziętara, M.S. (2018) Horizontal transmission of ectoparasite Gyrodactylus arcuatus (Monogenea, Gyrodactylidae) to the next generation of three-spined stickleback Gasterosteus aculeatus. Folia Parasitologica 65:006 (2018) | DOI: 10.14411/fp.2018.006

Lumme, J., Ziętara, M.S., Lebedeva, D. (2017) Ancient and modern genome shuffling: Reticulate mito-nuclear phylogeny of four related allopatric species of Gyrodactylus von Nordmann, 1832 (Monogenea: Gyrodactylidae), ectoparasites on the Eurasian minnow Phoxinus phoxinus L. (Cyprinidae). Systematic Parasitology 94: 183-200. DOI 10.1007/s11230-016-9696-y 

Lumme, J., Anttila, P., Rintamäki, P., Koski, P. Romakkaniemi, A. (2016) Genetic gradient of a host-parasite pair persisted ten years against physical mobility: Baltic Salmo salar vs. Gyrodactylus salaris. Infection, Genetics and Evolution, 45: 33-39 (available online Aug 6, 2016).

Lumme, J., Mäkinen, H.S., Ermolenko A.V., Gregg, J.L., Ziętara, M.S. (2016) Displaced phylogeographic signal of Gyrodactylus arcuatus, parasite of three-spined stickleback Gasterosteus aculeatus, suggest freshwater glacial refugia in Europe. International Journal for Parasitology 46: 545-554. 

Ieshko, E., Barskaya, Yu., Parshukov, A., Lumme, J. Khlunov, O. (2016) Occurrence and morphogenetic characteristics of Gyrodactylus (Monogenea: Gyrodactylidae) from a rainbow trout farm (Lake Ladoga, Russia). Acta Parasitologica 61: 151-157


Lumme, J., Ozerov, M., A. Veselov, C.R. Primmer. (2015) The formation of landlocked populations of Atlantic salmon. Pp. 26-43. In  " Evolutionary Biology of the Atlantic Salmon", eds. Tomislav Vladiĉ and Erik Petersson. CRC Press.

Ieshko, E., Lebedeva, D., Lumme, J. (2015) A new Gyrodactylus strain on brown trout (Salmo trutta) in Jänisjärvi, Russian Karelia, and a literature revision of salmonid parasites of the genus Gyrodactylus in  North-Western Russia and adjacent areas. Acta Parasitologica 60: 75-84.

Zueva K.J., J. Lumme, A.E. Veselov, M.P. Kent, S. Lien, C.R. Primmer (2014) Footprints of directional selection in wild Atlantic salmon populations: evidence for parasite-driven evolution? PLOSone March 26, 2014

Ozerov, M.Y., A.E. Veselov, J. Lumme and C.R. Primmer.(2013). Temporal variation of genetic composition in Atlantic salmon populations from the Western White Sea Basin: influence of anthropogenic factors? BMC Genetics14: 88–102.

Tolkkinen, M., H. Mykrä, A-M Markkola, H Aisala, K-M Vuori, J Lumme, AM Pirttilä, T Muotka (2013) Decomposer communities in human-impacted streams: species dominance rather than richness affects leaf decomposition. J. Applied Ecology 50: 1142-1151.

Ozerov, M., A. Veselov, J. Lumme and C.R. Primmer. (2012). “Riverscape” genetics: river characteristics influence the genetic structure and diversity of anadromous and freshwater Atlantic salmon (Salmo salar) populations in northwest Russia. Can. J. Fish. Aquat. Sci. 69: 947–1958.

Ziętara, M.S. , Lebedeva, D., Muñoz, G., Lumme, J. (2012) A monogenean fish parasite, Gyrodactylus chileani n.sp., belonging to a novel marine species lineage found in the South-Eastern Pacific and the Mediterranean and North Seas. Systematic Parasitology 83: 159-167.

Lumme, J. (2012) Lajiutumisesta, isäntäspesifiydestä ja isännänvaihdosta: Gyrodactylus-suvun loiset adaptiivisen evoluution esimerkkinä. Teoksessa ”Suomen kalojen loiset”, toimittajat E.T. Valtonen, T. Hakalahti-Sirén, A. Karvonen & K. Pulkkinen. Gaudeamus, Helsinki.

Valtonen, E.T. , T. Hakalahti-Sirén, T.,  Lumme, J. (2012) Pääjakso Laakamadot (Platyhelminthes): luokka Kidusmadot (Monogenea). Teoksessa ”Suomen kalojen loiset”, toimittajat E.T. Valtonen, T. Hakalahti-Sirén, A. Karvonen & K. Pulkkinen. Gaudeamus, Helsinki.

Ozerov M.Yu., Lumme J., Päkk P., Rintamäki P., Ziętara M.S., Barskaya Y., Lebedeva D., Saadre E. Gross R., Primmer C.R., Vasemägi A, (2010)  High Gyrodactylus salaris infection rate in triploid Atlantic salmon (Salmo salar L.). Diseases of Aquatic Organisms 91: 129-136

Ozerov MYu, Veselov AJe, Lumme J, Primmer CR (2010) Genetic structure of freshwater Atlantic salmon (Salmo salar) populations from the lakes Onega and Ladoga of northwest Russia and implications for conservation. Conservation Genetics 11: 1711-1724 

Tonteri A, Vasemägi A, Lumme J, Primmer CR (2010) Beyond MHC: signals of elevated selection pressure in Atlantic salmon (Salmo salar) immune relevant loci. Molecular Ecology 19: 1273-1282.

Ziętara MS, Rokicka M, Stojanovski S, Lumme J (2010) Introgression of distant mitochondria into the genome of Gyrodactylus salaris: Nuclear and mitochondrial markers are necessary to identify parasite strains. Acta Parasitologica 55: 20-28.

Калюжин С.М, Веселов А. Е., Лумме Я. И. (2009) Лососевые реки полуострова Рыбачий.  Петрозаводск, изл-во КарНЦ РАН. 180 с. ISBN 978-5-9274-0382-0

Rokicka M, Lumme J, Ziętara MS (2009) Two new Antarctic Gyrodactylus species (Monogenoidea): description and phylogenetic characterization. J. Parasitology 95: 1112-1119.

Tonteri A, Veselov AJe, Zubchenko AV, Lumme J, Primmer, CG (2009) Microsatellites reveal clear genetic boundaries among Atlantic salmon (Salmo salar) populations from the Barents and White Seas, northwest Russia. Canadian J. Fisheries and Aquatic Sciences 66: 717-735.

Kuusela J, Holopainen R, Meinilä M, Anttila P, Koski P, Ziętara MS, Veselov AJe, Primmer CR, Lumme J (2009) Clonal structure of salmon parasite Gyrodactylus salaris on a coevolutionary gradient on Fennoscandian salmon (Salmo salar). Ann. Zool. Fenn. 46: 21-33.

Tonteri A, Vasemägi A, Lumme J,  Primmer CR (2008) Use of differential expression data for identification of novel immune relevant EST-linked microsatellite markers in Atlantic salmon (Salmo salar L.) Molecular Ecology Resources 8: 1486-1490.

Kuusela J, Zietara MS, Lumme J (2008) Description of three new European cryptic species of Gyrodactylus supported by nuclear and mitochondrial phylogenetic chracaterization. Acta Parasitologica 53: 120-126.

Ziętara MS, Kuusela J, Veselov AJe, Lumme J (2008). Molecular faunistics of accidental infections of Gyrodactylus Nordmann, 1832 (Monogenea) parasitic on salmon Salmo salar L. and brown trout Salmo trutta L. in NW Russia. Systematic Parasitology 69: 123-135.

Ziętara MS, Johnsen, BO, Lumme J (2008) Genetisk analyse av opprinnelsen ti Gyrodactylus salaris-infeksjonen på laksunger i Laerdalselva. NINA Rapport 371.

Kuusela J,  Ziętara MS, Lumme J (2007). Hybrid origin of Baltic salmon-specific parasite Gyrodactylus salaris: a model for speciation by host switch for hemiclonal organisms. Molecular Ecology 16: 5234-5245.

Rokicka M, Lumme J, Ziętara MS (2007). Identification of Gyrodactylus ectoparasites in Polish salmonid farms by PCR-RFLP of the nuclear ITS segment of ribosomal DNA (Monogenea: Gyrodactylidae). Acta Parasitologica 52: 185-195.

Tonteri A, Veselov AJe, Titov S, Lumme J, Primmer CR (2007) The effect of migratory behaviour on genetic diversity and population divergence: a comparison of anadromous and freshwater Atlantic salmon Salmo salar. Journal of Fish Biology 70: 381-398.

Ziętara MS, Kuusela J, Lumme J (2006). Escape from an evolutionary dead-end: a triploid clone of Gyrodactylus salaris is able to revert to sex and switch host (Platyhelminthes, Monogenea, Gyrodactylidae). Hereditas 143, 86-92.

Tonteri A, Titov S, Veselov A, Zubchenko A, Koskinen MT, Lesbarrères D, Kaluzchin S, Bakhmet I, Lumme J, Primmer CR (2005) Phylogeography of anadromous and non-anadromous Atlantic salmon (Salmo salar) from northern Europe. - Ann. Zool. Fenn. 45: 1- 22.

Ziętara M, Lumme J (2004) Comparison of molecular phylogeny and morphological systematics in fish parasite genus Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae). - Zoologica Poloniae 49: 5-28.

Ruokonen M, Kvist L, Arvak T, Gang L, Iwabuchi S, Markkola J, Morozov V, Öien IJ, Syroechkovsky EJr, Tolvanen P, Lumme J (2004) Phylogeography and population genetic structure of the endangered lesser white-fronted goose (Anser erythropus) - Conservation Genetics, 5: 501-512.

Asplund T, Veselov A, Primmer CR, Bakhmet I, Potutkin A, Titov, S, Zubchenko A, Studenov I, Kaluzchin S, Lumme J (2004) Geographical structure and postglacial history of mtDNA haplotype variation in Atlantic salmon (Salmo salar L.) among rivers of the White and Barents Sea basins.- Ann. Zool. Fenn. 44: 465-475.

Meinilä M, Kuusela J, Ziętara MS, Lumme J (2004) Initial steps of speciation by geographic isolation and host switch in salmonid pathogen Gyrodactylus salaris (Monogenea: Gyrodactylidae). Int. J. Parasitol. 34: 515-526.

Ziętara  M, Lumme J (2003) The crossroads of molecular, typological and biological species concept: two new species of Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae). - Systematic Parasitology 55: 39-52.

Uimaniemi, L, Orell, M, Kvist, L, Jokimäki, J, Lumme, J (2003) Genetic variation of the Siberian Tit (Parus cinctus) populations at the regional level: A mitochondrial sequence analysis. - Ecography 26: 98-106.

Gross R, Nilsson J, Kohlman K, Lumme J, Titov S, Veselov AJe (2003) Distribution of growth hormone 1 gene haplotypes among Atlantic salmon, Salmo salar L. populations in Europe. In: Atlantic salmon: biology, conservation and restoration. Petrozavodsk, Karelian Research Centre of RAS,  pp. 32-37.

Ziętara M, Lumme J (2002) Speciation by host switch and adaptive radiation in fish parasite genus Gyrodactylus (Platyhelminthes, Monogenea). -Evolution 56: 2445-2458.

Meinilä M, Kuusela J, Zietara M, Lumme J (2002) Primers for amplifying  ~800 bp of highly polymorphic mitochondrial COI gene of Gyrodactylus salaris (Platyhelminthes, Monogenea, Gyrodactylidae) - Hereditas 137: 72-74.

Liukkonen-Anttila T, Uimaniemi L, Orell M, Lumme J (2002) Mitochondrial DNA variation and the phylogeography of the grey partridge (Perdix perdix) in Europe: from Pleistocene history to present day populations. - J. Evol. Biol. 15: 971-982.

Ziętara, MS, Huyse T, Lumme J, Volckaert FA (2002) Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. - Parasitology 124: 39-52.

Lumme J, Ruokonen M, Liukkonen-Anttila T (2002) DNA:n sekvensointi populaatiotutkimuksessa - esimerkkeinä kiljuhanhi ja peltopyy. - Suomen Riista 48: 90-97.

Nilsson J, Gross R, Asplund T, Dove O, Jansson H, Kelloniemi J, Kohlman K, Löytynoja A, Nielsen EE, Paaver T, Primmer CR, Titov S, Vasemägi A, Veselov A, Öst T, Lumme J (2001) Matrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea area. - Molecular Ecology  10: 89-102.

Veselov AJe, Lumme J, Bakhmet IN, Primmer CR, Titov SF, Koskinen MT, Potutkin AG. (2001) Salmon rivers of the White sea and Onega lake basins. (2001). In: Biogeography of Karelia. Petrozavodsk, Karelian Research Centre of RAS, pp. 152-166. (in Russian)

Ruokonen M, Kvist L, Tegelström H, Lumme J (2000) Goose hybrids, captive breeding and restocking of the Fennoscandian Lesser White-fronted goose (Anser erythropus). - Conservation Genetics 1: 277-283.

Uimaniemi L, Orell M, Mönkkönen M, Huhta E, Jokimäki J, Lumme J (2000) Genetic diversity in the Siberian Jay (Perisoreus infaustus) in fragmented old-growth forests in Fennoscandia. - Ecography 23: 669-677.

Ruokonen M, Kvist L, Lumme J (2000) Close relatedness between mitochondrial DNA from seven Anser goose species. - J. Evol. Biol. 13: 532-540.

Hoikkala A, Päällysaho S, Aspi J, Lumme J (2000) Localization of genes affecting species differences in male courtship song between Drosophila virilis and D. littoralis. - Genetical Research 75: 37-45.

Kvist L, Ruokonen M, Lumme J,  Orell M (1999) The colonization history and present-day population structure of the European great tit (Parus major major). - Heredity 82: 495-502.

Kvist L, Ruokonen M, Lumme J, Orell M (1999) Different population structures in northern and southern populations of the European blue tit (Parus caeruleus) - J. Evol. Biol 12: 798-805.

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