DNA Identification of Parasitic Copepods Salmincola (Copepoda, Siphonostomatoida, Lernaeopodidae): Variability and Rate of Evolution of the Mitochondrial Cytochrome c Oxidase Subunit I Gene

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Abstract

The barcode fragment of the COI gene was sequenced in 91 specimens of five species of parasitic Salmincola copepods, sampled from salmonids mainly from the Russian Far East: S. californiensis (mykiss and masu salmon) and S. edwardsii (various species of chars, sockeye salmon from Lake Kronotskoe), S. carpionis (various species of chars), S. markewitschi (whitespotted char), S. stellata (Sakhalin taimen). A total of 41 haplotypes were found with a maximum level of differences of 0.183 nucleotide substitutions per position. The distance between species varied from 0.139 ± 0.014 in the S. markewitschiS. carpionis pair to 0.179 ± 0.015 in the S. stellataS. californiensis pair. The intraspecific nucleotide diversity of the COI gene fragment is much lower: for S. californiensis and S. edwardsii, inhabiting the gill cavity and fins of the host – 0.013 ± 0.003 and 0.015 ± 0.003, and for S. stellata, S. markewitschi, and S. carpionis, localized in the buccal cavity of the hosts – 0.002 ± 0.001, 0.004 ± 0.001, and 0.005 ± 0.001, respectively. A comparison of samples of three Salmincola copepod species from different regions of the Russian Far East revealed a significant (Fst = 0.28–0.42, P \( \ll \) 0.001) genetic subdivision. Three subclades of edwardsii-like copepods – S. edwardsii from the Russian Far East, S. edwardsii from the American brook char of eastern North America, and S. siscowet from the lake char of Michigan (COI sequences of copepods from the last two groups are taken from genetic databases) – differed from each other by an average of 9.3–10.9% nucleotide positions, which means the need for a taxonomic revision of S. edwardsii. According to the molecular dating carried out, the divergence of Salmincola lineages started in the Miocene and ended in the early Pliocene. The phylogenetic substitution rate was 0.0228 (95% interval: 0.0132–0.033) nucleotide substitutions/position/million years/lineage. The rate of nucleotide substitutions at the population level is 3.7 times higher – 0.0849 (0.0212–0.170). The high level of variability of the COI gene fragment makes this marker a useful tool both for developing the taxonomy and phylogeny of Salmincola and Lernaeopodidae copepods at the species and genus levels, and for analyzing the differentiation of their populations.

About the authors

S. V. Shedko

Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far East Branch of the Russian Academy of Sciences

Author for correspondence.
Email: shedko@biosoil.ru
Russia, 690022, Vladivostok

M. B. Shedko

Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far East Branch of the Russian Academy of Sciences

Email: shedko@biosoil.ru
Russia, 690022, Vladivostok

I. L. Miroshnichenko

Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far East Branch of the Russian Academy of Sciences

Email: shedko@biosoil.ru
Russia, 690022, Vladivostok

G. A. Nemkova

Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far East Branch of the Russian Academy of Sciences

Email: shedko@biosoil.ru
Russia, 690022, Vladivostok

References

  1. Bernot J.P., Boxshall G.A., Crandall K.A. A synthesis tree of the Copepoda: Integrating phylogenetic and taxonomic data reveals multiple origins of parasitism // Peer J. 2021. V. 9. e12034. https://doi.org/10.7717/PEERJ.12034/SUPP-2
  2. Walter T.C., Boxshall G. World of Copepods Database. Lernaeopodidae Milne Edwards, 1840. 2023. World Register of Marine Species. Пpocмoтpeнo 12.04.2023. https://www.marinespecies.org/aphia.php?p=taxdetails&id=135525
  3. Kabata Z. Parasitic Copepoda of British Fishes. London: The Ray Society, 1979. V. 152. 468 p.
  4. Kabata Z. Revision of the genus Salmincola Wilson, 1915 (Copepoda: Lernaeopodidae) // J. Fish. Res. Board Can. 1969. V. 26. P. 2987–3041. https://doi.org/10.1139/z86-276
  5. Kabata Z. Copepoda and Branchiura // Guide to the Parasites of Fishes of Canada. Part II. Crustacea / Eds Margolis L., Kabata Z. Ottava: Dept. Fisheries and Oceans, 1988. P. 3–128.
  6. Hare G.M., Frantsi C. Abundance and potential pathology of parasites infecting salmonids in Canadian Maritime hatcheries // J. Fish. Res. Board Can. 1974. V. 31. P. 1031–1036. https://doi.org/10.1139/f74-11
  7. Bell G.R., Margolis L. The fish health program and the occurrence of fish diseases in the Pacific region of Canada // Fish Pathology. 1976. V. 10. № 2. P. 115–122. https://doi.org/10.3147/jsfp.10.115
  8. Kabata Z., Cousens B. Host-parasite relationships sockeye salmon, Oncorhynchus nerka, and Salmincola californiensis (Copepoda: Lernaeopodidae) // J. Fish. Res. Board Can. 1977. V. 34. P. 191–202. https://doi.org/10.1139/f77-02
  9. Johnson K.A., Heindel J.A. Efficacy of manual removal and ivermectin gavage for control of Salmincola californiensis (Wilson) infestation of chinook salmon, Oncorhynchus tschawytscha (Walbaum), captive broodstocks // J. Fish Diseases. 2001. V. 24. P. 197–203. https://doi.org/10.1046/j.1365-2761.2001.00279.x
  10. Roberts R.J., Johnson K.A., Casten M.T. Control of Salmincola californiensis (Copepoda: Lernaeopodidae) in rainbow trout, Oncorhynchus mykiss (Walbaum): A clinical and histopathological study // J. Fish Diseases. 2004. V. 27. P. 73–79.
  11. Piasecki W., Goodwin A.E., Eiras J.C., Nowak B.F. Importance of Copepoda in freshwater aquaculture // Zool. Studies. 2004. V. 43. № 2. P. 193–205.
  12. Mitro M. Brook trout, brown trout, and ectoparasitic copepods Salmincola edwardsii: Species interactions as a proximate cause of brook trout loss under changing environmental conditions // Transactions of the Am. Fisheries Society. 2016. V. 145. № 6. P. 1223–1233. https://doi.org/10.1080/00028487.2016.1219676
  13. Ratnasingham S., Hebert P.D.N. BOLD: The barcode of life data system (http://www.barcodinglife.org) // Mol. Ecol. Notes. 2007. V. 7. № 3. P. 355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x
  14. Маркевич А.П. Паразитические веслоногие рыб СССР. Киев: Изд-во АН УССР, 1956. 260 с.
  15. Гусев А.В. Тип Членистоногие – Arthropoda // Определитель паразитов пресноводных рыб фауны СССР. Т. 3. Паразитические многоклеточные (Вторая часть). Л.: Наука, 1987. С. 378–524.
  16. Шедько М.Б., Шедько С.В. О паразитических копеподах рода Salmincola (Lernaeopodidae) от дальневосточных гольцов Salvelinus (Salmonidae) с описанием нового вида Salmincola markewitschi sp. n. // Зоол. журн. 2002. Т. 81. № 2. С. 141–153.
  17. Шедько М.Б., Шедько С.В. Распространение и морфология Salmincola stellatus (Copepoda: Lernaeopodidae) от сахалинского тайменя Parahucho perryi (Salmonidae) из Приморья // Паразитология. 2003. Т. 37. Вып. 1. С. 60–68.
  18. Шедько М.Б. Фауна паразитических копепод рода Salmincola (Lernaeopodidae) рыб Камчатки // Сохранение биоразнообразия Камчатки и прилегающих морей: Доклады V научной конф. Петропавловск-Камчатский: Камчатпресс, 2005. С. 128–139.
  19. Шедько М.Б., Поспехов В.В., Атрашкевич Г.И. Новые данные по фауне пресноводных паразитических копепод рода Salmincola (Copepoda: Lernaeopodidae) рыб северо-западной части побережья Охотского моря // Чтения памяти В.Я. Леванидова. Вып. 3. Владивосток: Дальнаука, 2005. С. 421–434.
  20. Шедько М.Б., Шедько С.В., Виноградов С.А. Фауна пресноводных паразитических копепод семейства Lernaeopodidae (Crustacea: Copepoda) рыб острова Сахалин // Растительный и животный мир острова Сахалин (Материалы Международного сахалинского проекта). Часть 2. Владивосток: Дальнаука, 2005. С. 52–63.
  21. Соколов С.Г., Шедько М.Б., Протасова Е.Н., Фролов Е.В. Паразиты рыб внутренних водоемов острова Сахалин // Растительный и животный мир островов северо-западной части Тихого океана (Матер. Междунар. Курильского и Междунар. сахалинского проектов). Владивосток: Дальнаука, 2012. С. 179–216.
  22. Kabata Z. Redescriptions of and comments on four little-known Lernaeopodidae (Crustacea: Copepoda) // Can. J. Zool. 1986. V. 64. P. 1852–1859. https://doi.org/10.1139/z86-276
  23. Nagasawa K., Urawa S. New records of the parasitic copepod Salmincola stellatus from Sakhalin taimen (Hucho perryi) in Hokkaido, with a note on its attachment site // Sci. Rep. Hokkaido Salmon Hatchery. 1991. V. 45. P. 57–59.
  24. Nagasawa K. Salmincola markewitsehi (Copepoda: Lernaeopodidae) parasitic on whitespotted char, Salvelinus leucomaenis, in a mountain stream of Honshu Island, Central Japan // Species Divers. 2020. V. 25. № 2. P. 369–375. https://doi.org/10.12782/ specdiv.25.369
  25. Nagasawa K. Two Copepods Salmincola edwardsii and Salmincola markewitschi (Lernaeopodidae) parasitic on chars (Salvelinus spp.) reared in a salmon museum, Northern Japan // Species Divers. 2021. V. 26. № 2. P. 137–143. https://doi.org/10.12782/specdiv.26.137
  26. Nagasawa K., Urawa S. Occurrence of Salmincola edwardsii (Olsson, 1869) and Salmincola markewitschi Shedko & Shedko, 2002 (Copepoda: Lernaeopodidae) on stream-dwelling salmonids in eastern Hokkaido, Japan, with observations on the morphology of the copepods // Crustac. Res. 2022. V. 51. P. 91–101. https://doi.org/10.18353/crustacea.51.0_91
  27. Aljanabi S.M., Martinez I. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques // Nucl. Ac. Res. 1997. V. 25. № 22. P. 4692–4693. https://doi.org/10.1093/nar/25.22.4692
  28. Folmer O., Black M., Hoeh W. et al. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates // Mol. Mar. Biol. Biotechnol. 1994. V. 3. № 5. P. 294–299.
  29. Staden R., Beal K.F., Bonfield J.K. The Staden Package, 1998 // Bioinform. Methods Protoc. 2000. V. 132. P. 115–130. https://doi.org/10.1385/1-59259-192-2:115
  30. Gouy M., Guindon S., Gascuel O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building // Mol. Biol. Evol. 2010. V. 27. № 2. P. 221–224. https://doi.org/10.1093/molbev/msp259
  31. Nguyen L.-T., Schmidt H.A., von Haeseler A., Minh B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies // Mol. Biol. Evol. 2015. V. 32. № 1. P. 268–274. https://doi.org/10.1093/molbev/msu300
  32. Chernomor O., von Haeseler A., Minh B.Q. Terrace aware data structure for phylogenomic inference from supermatrices // Syst. Biol. 2016. V. 65. № 6. P. 997–1008. https://doi.org/10.1093/sysbio/syw037
  33. Hoang D.T., Chernomor O., von Haeseler A. et al. UFBoot2: Improving the ultrafast bootstrap approximation // Mol. Biol. Evol. 2018. V. 35. № 2. P. 518–522. https://doi.org/10.1093/molbev/msx281
  34. Drummond A.J., Suchard M.A., Xie D., Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7 // Mol. Biol. Evol. 2012. V. 29. № 8. P. 1969–1973. https://doi.org/10.1093/molbev/mss075
  35. Swofford D.L. PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Version 4.0. Sunderland, Mass.: Sinauer Assoc., 2002.
  36. Nei M. Molecular Evolutionary Genetics. N.Y.: Columbia Univ. Press, 1987. 512 p.
  37. Nei M., Jin L. Variances of the average numbers of nucleotide substitutions within and between populations // Mol. Biol. Evol. 1989. V. 6. № 3. P. 240–300. https://doi.org/10.1093/oxfordjournals.molbev.a040547
  38. Excoffier L., Lischer H.E.L. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows // Mol. Ecol. Resources. 2010. V. 10. P. 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
  39. Шедько С.В., Мирошниченко И.Л., Немкова Г.А. Филогения лососевых рыб (Salmoniformes: Salmonidae) и ее молекулярная датировка: анализ мтДНК-данных // Генетика. 2013. Т. 49. № 6. С. 718–734. https://doi.org/10.7868/S0016675813060118
  40. Lecaudey L.A., Schliewen U.K., Osinov A.G. et al. Molecular phylogenetics and evolution inferring phylogenetic structure, hybridization and divergence times within Salmoninae (Teleostei: Salmonidae) using RAD-sequencing // Mol. Phylogenet. Evol. 2018. V. 124. P. 82–99. https://doi.org/10.1016/j.ympev.2018.02.022
  41. Cavender T.M., Miller R.R. Smilodonichthys rastrosus, a new Pliocene salmonid fish from western United States // Bull. of the Oregon Museum of Natural History. 1972. V. 18. P. 1–44.
  42. Eiting T.P., Smith G.R. Miocene salmon (Oncorhynchus) from Western North America: Gill Raker evolution correlated with plankton productivity in the Eastern Pacific // Palaeogeogr. Palaeoclimatol. Palaeoecol. 2007. V. 249. № 3–4. P. 412–424. https://doi.org/10.1016/j.palaeo.2007.02.011
  43. Loeza-Quintana T., Carr C.M., Khan T. et al. Recalibrating the molecular clock for Arctic marine invertebrates based on DNA barcodes // Genome. 2019. V. 62. № 3. P. 200–216. https://doi.org/10.1139/gen-2018-0107
  44. Ho S.Y.W., Phillips M.J., Cooper A., Drummond A.J. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times // Mol. Biol. Evol. 2005. V. 22. № 7. P. 1561–1568. https://doi.org/10.1093/molbev/msi145
  45. Шедько С.В. Скорость эволюции митохондриального гена цитохрома b согласно анализу недавней (около 12000 лет) изоляции гольцов Salvelinus озера Кроноцкое // Генетика. 2019. Т. 55. № 12. С. 1466–1470. https://doi.org/10.1134/S0016675819090157
  46. Forster P., Harding R., Torroni A., Bandelt H.-J. Origin and evolution of native american mtDNA variation: A reappraisal // Am. J. Hum. Genet. 1996. V. 59. № 4. P. 935–945.
  47. Canty A., Ripley B. boot: Bootstrap R (S-Plus) Functions. R package version 1.3-20. 2017. 117 p.
  48. Мелекесцев И.В., Брайцева О.А., Эрлих Э.Н., Кожемяка Н.Н. Вулканические горы и равнины // История развития рельефа Сибири и Дальнего Востока. Камчатка, Курильские и Командорские острова. М.: Наука, 1974. С. 162–233.
  49. Гущенко И.И. Вулкан Кроноцкий // Действующие вулканы Камчатки. М.: Наука, 1991. Т. 2. С. 52–61.
  50. Harigai W., Saito A., Suzuki H., Yamamoto M. Genetic diversity of Ligidium isopods in Hokkaido and Niigata, Northern Japan, based on mitochondrial DNA analysis // Zoolog. Sci. 2020. V. 37. № 5. P. 417–428. https://doi.org/10.2108/zs200017
  51. Crandall E.D., Sbrocco E.J., De Boer T.S. et al. Expansion dating: Calibrating molecular clocks in marine species from expansions onto the Sunda Shelf following the last glacial maximum // Mol. Biol. Evol. 2012. V. 29. № 2. P. 707–719. https://doi.org/10.1093/MOLBEV/MSR227

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