Different hosts in different lakes: prevalence and population genetic structure of plerocercoids of Ligula intestinalis (Cestoda) in Czech water bodies.
Czech Republic
fish parasite
freshwater
host specificity
tapeworm
Journal
Folia parasitologica
ISSN: 1803-6465
Titre abrégé: Folia Parasitol (Praha)
Pays: Czech Republic
ID NLM: 0065750
Informations de publication
Date de publication:
15 Sep 2022
15 Sep 2022
Historique:
received:
29
10
2021
accepted:
26
04
2022
entrez:
3
10
2022
pubmed:
4
10
2022
medline:
5
10
2022
Statut:
epublish
Résumé
Ligula intestinalis (Linnaeus, 1758) is a tapeworm parasite with a worldwide distribution that uses a wide variety of fish species as its second intermediate host. In the present study, we investigated the prevalence and population genetic structure of plerocercoids of L. intestinalis in five common cyprinoid species, roach Rutilus rutilus (Linnaeus), freshwater bream Abramis brama (Linnaeus), white bream Blicca bjoerkna (Linnaeus), bleak Alburnus alburnus (Linnaeus), and rudd Scardinius erythrophthalmus (Linnaeus), collected in six water bodies of the Czech Republic (Milada, Most, Medard, Jordán, Římov and Lipno). Of the six study sites, the highest frequency of parasitism was recorded in Lake Medard (15%). The overall prevalence rate among the species was as follows: roach > rudd ≥ freshwater bream > bleak > white bream. Two mitochondrial genes (cytb and COI) were used to compare the population genetic structure of parasite populations using selected samples from the five fish species. The results of the phylogenetic analysis indicated that all populations of L. intestinalis were placed in Clade A, previously identified as the most common in Europe. At a finer scale, haplotype network and PCoA analyses indicated the possible emergence of host specificity of several mtDNA haplotypes to the freshwater bream. Moreover, pairwise Fixation indices (F
Identifiants
pubmed: 36185031
doi: 10.14411/fp.2022.018
doi:
pii:
Substances chimiques
DNA, Mitochondrial
0
Water
059QF0KO0R
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Références
Appelberg M., Berger H.-M., Hesthagen T., Kleiven E., Kurkilahti M., Raitaniemi J., Rask M. 1995: Development and intercalibration of methods in Nordic freshwater fish monitoring. Water. Air. Soil Pollut. 85: 401-406.
doi: 10.1007/BF00476862
Arme C., Owen R.W. 1968: Occurrence and pathology of Ligula intestinalis infections in British fishes. J. Parasitol. 54: 272-280.
pubmed: 5647108
doi: 10.2307/3276934
Barson M., Marshall B.E. 2003: The occurrence of the tapeworm Ligula intestinalis (L.), in Barbus paludinosus from a small dam in Zimbabwe. African J. Aquat. Sci. 28: 175-178.
doi: 10.2989/16085910309503782
Baruš V., Prokeš M. 1995: Length-weight relationship of Ligula intestinalis plerocercoids in adult silver bream and discussion on estimation of the parasite age. Appl. Parasitol. 36: 192-199.
pubmed: 8541892
Bean C.W., Winfield I.J. 1991: Influences of the tapeworm Ligula intestinalis (L.) on the spatial distributions of juvenile roach Rutilus rutilus (L.) and gudgeon Gobio gobio (L.) in Lough Neagh, Northern Ireland. Netherlands J. Zool.42: 419-429.
doi: 10.1163/156854291X00423
Bernard M.S., Strittmatter M., Murúa P., Heesch S., Cho G.Y., Leblanc C., Peters A.F. 2019: Diversity, biogeography and host specificity of kelp endophytes with a focus on the genera Laminarionema and Laminariocolax (Ectocarpales, Phaeophyceae). Eur. J. Phycol. 54: 39-51.
doi: 10.1080/09670262.2018.1502816
Blabolil P., Boukal D.S., Ricard D., Kubečka J., Říha M., Vašek M., Prchalová M., Čech M., Frouzová J., Jůza T., Muška M., Tušer M., Draštík V., Šmejkal M., Vejřík L., Peterka J. 2017: Optimal gillnet sampling design for the estimation of fish community indicators in heterogeneous freshwater ecosystems. Ecol. Indic. 77: 368-376.
doi: 10.1016/j.ecolind.2017.02.036
Blatrix R., Herbers J.M. 2003: Coevolution between slave-making ants and their hosts: host specificity and geographical variation. Mol. Ecol. 12: 2809-2816.
pubmed: 12969483
doi: 10.1046/j.1365-294X.2003.01947.x
Blouin M.S. 2002: Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int. J. Parasitol. 32: 527-531.
doi: 10.1016/S0020-7519(01)00357-5
Bouzid W., Lek S., Mace M., Ben Hassine O., Etienne R., Legal L., Loot G. 2008a: Genetic diversity of Ligula intestinalis (Cestoda: Diphyllobothriidea) based on analysis of inter-simple sequence repeat markers. J. Zool. Syst. Evol. Res. 46: 289-296.
doi: 10.1111/j.1439-0469.2008.00471.x
Bouzid W., Štefka J., Bahri-Sfar L., Beerli P., Loot G., Lek S., Haddaoui N., Hypša V., Scholz T., Dkhil-Abbes T. 2013: Pathways of cryptic invasion in a fish parasite traced using coalescent analysis and epidemiological survey. Biol. Invasions 15: 1907-1923.
doi: 10.1007/s10530-013-0418-y
Bouzid W., Štefka J., Hypša V., Lek S., Scholz T., Legal L., Hassine O.K. Ben, Loot G. 2008b: Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). Int. J. Parasitol. 38: 1465-1479.
doi: 10.1016/j.ijpara.2008.03.008
Britton J.R., Jackson M.C., Harper D.M. 2009: Ligula intestinalis (Cestoda: Diphyllobothriidae) in Kenya: a field investigation into host specificity and behavioural alterations. Parasitology 136: 1367-1373.
pubmed: 19627635
doi: 10.1017/S003118200999059X
Brown S.P., Loot G., Grenfell B.T., Guégan J.F. 2001: Host manipulation by Ligula intestinalis: accident or adaptation? Parasitology 123: 519.
pubmed: 11719963
doi: 10.1017/S0031182001008678
Bykhovskaya-Pavlovskaya I.E. 1964: Key to Parasites of Freshwater Fish of the USSR. Israel Program for Scientific Translations, Jerusalem, 919 pp.
Carter B.C., Shubeita G.T., Gross S.P. 2005: Tracking single particles: a user-friendly quantitative evaluation. Phys. Biol. 2: 60.
doi: 10.1088/1478-3967/2/1/008
Chapman A., Hobbs R.P., Morgan D.L., Gill H.S. 2006: Helminth parasitism of Galaxias maculatus (Jenyns, 1842) in southwestern Australia. Ecol. Freshw. Fish. 15: 559-564.
doi: 10.1111/j.1600-0633.2006.00198.x
Cole R., Viney M. 2019: Correction to: The population genetics of parasitic nematodes of wild animals. Parasit. Vectors. 12: 1.
pubmed: 30606222
doi: 10.1186/s13071-019-3731-1
Dence W.A. 1958: Studies on Ligula-infected common shiners (Notropis cornutus frontalis Agassiz) in the Adirondacks. J. Parasitol 44: 334-338.
pubmed: 13550029
doi: 10.2307/3274601
Dubinina M.N. 1980: Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. Amerind Publishing Company, Delhi, 320 pp.
Ergonul M.B., Altindag A. 2005: The occurrence and dynamics of Ligula intestinalis in its cyprinid fish host, tench, Tinca tinca, in Mogan Lake (Ankara, Turkey). Vet. Med. 50: 537.
doi: 10.1501/0000108
Groves K.L., Shields B.A. 2001: Observations on the plerocercoid stage of the tapeworm Ligula in three species of fish from the lower Crooked River of central Oregon. J. Aquat. Anim. Health. 13: 285-289.
doi: 10.1577/1548-8667(2001)013<0285:OOTPSO>2.0.CO;2
Hoang D.T., Chernomor O., von Haeseler A., Minh B.Q., Vinh L.S. 2018: UFBoot2: Improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35: 518-522.
pubmed: 29077904
doi: 10.1093/molbev/msx281
Holmes J.C., Bethel W.M. 1972: Modification of intermediate host behavior by parasites. In: E.U. Canning and C.A. Wright (Eds.), Behavioral Aspects of Parasite Transmission, Academic Press, New York, pp. 128-149.
Huyse T., Poulin R., Théron A., Theron A. 2005: Speciation in parasites: a population genetics approach. Trends Parasitol. 21: 469-475.
pubmed: 16112615
doi: 10.1016/j.pt.2005.08.009
Ivankov V.N., Kaplunenko V.A., Bol'shakov S.G., Zheleznova L. V. 2020: First detections of the tapeworm Ligula intestinalis (Linnaeus, 1758) (Cestoda: Ligulidae) in the anadromous far eastern redfin Tribolodon hakonensis (Gunther, 1880) (Teleostei: Cyprinidae) in Primorye. Russ. J. Mar. Biol. 46: 230-231.
doi: 10.1134/S1063074020030074
Iwanowicz D.D. 2011: Overview on the effects of parasites on fish health. In: R.C. Cipriano, A.W. Bruckner and I.S. Shchelkunov (Eds.), Proceedings of the Third Bilateral Conference between Russia and the United States, Aquatic Animal Health 2009, Shepherdstown, 12-20 July 2009. Khaled bin Sultan Living Oceans Foundation, Landover, pp. 176-184.
Jombart T. 2008: adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403-1405.
pubmed: 18397895
doi: 10.1093/bioinformatics/btn129
Kennedy C.R. 1974: A checklist of British and Irish freshwater fish parasites with notes on their distribution. J. Fish Biol. 6: 613-644.
doi: 10.1111/j.1095-8649.1974.tb05104.x
Kennedy C.R., Burrough R.J. 1981: The establishment and subsequent history of a population of Ligula intestinalis in roach Rutilis rutilis (L.). J. Fish Biol. 19: 105-126.
doi: 10.1111/j.1095-8649.1981.tb05815.x
Kennedy C.R., Shears P.C., Shears J.A. 2001: Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology 123: 257-269.
pubmed: 11578089
doi: 10.1017/S0031182001008538
Kočová P. 2018: [Population-genomic analysis of adaptation in a parasite with a wide host range - tapeworm Ligula intestinalis.] Master thesis, University of South Bohemia in České Budějovice. (In Czech.)
Lagrue C., Presswell B., Dunckley N., Poulin R. 2018: The invasive cestode parasite Ligula from salmonids and bullies on the South Island, New Zealand. Parasitol. Res. 117: 151-156.
pubmed: 29177582
doi: 10.1007/s00436-017-5684-7
Lanfear R., Frandsen P.B., Wright A.M., Senfeld T., Calcott B. 2017: Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34: 772-773.
pubmed: 28013191
doi: 10.1093/molbev/msw260
Leigh J.W., Bryant D. 2015: POPART: Full-feature software for haplotype network construction. Methods Ecol. Evol. 6: 1110-1116.
doi: 10.1111/2041-210X.12410
Levron C., Sitko J., Scholz T. 2009: Spermiogenesis and spermatozoon of the tapeworm Ligula intestinalis (Diphyllobothriidea): phylogenetic implications. J. Parasitol. 95: 1-9.
pubmed: 18576887
doi: 10.1645/GE-1646.1
Li J., Liao X., Yang H. 2000: Molecular characterization of a parasitic tapeworm (Ligula) based on DNA sequences from formalin-fixed specimens. Biochem. Genet. 38: 309-322.
pubmed: 11129525
doi: 10.1023/A:1002009117626
Librado P., Rozas J. 2009: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
pubmed: 19346325
doi: 10.1093/bioinformatics/btp187
Longshaw M., Frear P.A., Nunn A.D., Cowx I.G., Feist S.W. 2010: The influence of parasitism on fish population success. Fish. Manag. Ecol. 17: 426-434.
doi: 10.1111/j.1365-2400.2010.00741.x
Loot G., Francisco P., Santoul F., Lek S., Guégan J.-F. 2001: The three hosts of the Ligula intestinalis (Cestoda) life cycle in Lavernose-Lacasse gravel pit, France. Arch. Hydrobiol. 152: 511-525.
doi: 10.1127/archiv-hydrobiol/152/2001/511
Martinů J., Hypša V., Štefka J. 2018: Host specificity driving genetic structure and diversity in ectoparasite populations: coevolutionary patterns in Apodemus mice and their lice. Ecol. Evol. 8: 10008-10022.
pubmed: 30397443
doi: 10.1002/ece3.4424
Meinilä M., Kuusela J., Ziętara M.S., 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.
doi: 10.1016/j.ijpara.2003.12.002
Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., von Haeseler A., Lanfear R. 2020: IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37: 1530-1534.
pubmed: 32011700
doi: 10.1093/molbev/msaa015
Ministry of Agriculture of the Czech Republic 2019: Report on Water Management in the Czech Republic in 2019, Accessed April 25, 2022, https://eagri.cz/Report
Moravec F., Scholz T. 2016: Helminth parasites of the lesser great cormorant Phalacrocorax carbo sinensis from two nesting regions in the Czech Republic. Folia Parasitol. 63: 022.
doi: 10.14411/fp.2016.022
Morgan D.L. 2003: Distribution and biology of Galaxias truttaceus (Galaxiidae) in south-western Australia, including first evidence of parasitism of fishes in Western Australia by Ligula intestinalis (Cestoda). Environ. BioL. Fishes. 66:155-167.
doi: 10.1023/A:1023645506913
Nazarizadeh M., Martinů J., Nováková M., Stanko M., Štefka J. 2022: Phylogeography of the parasitic mite Laelaps agilis in Western Palearctic shows lineages lacking host specificity but possessing different demographic histories. BMC Zool. 7: 15.
doi: 10.1186/s40850-022-00115-y
Nezafat R.B., Khara H., Satari M. 2008: Parasite infection of bream (Abramis brama orientalis Berg, 1949) in Aras Dam lake. J. Biol. Sci. 2: 83-96.
Nosil P. 2012: Ecological Speciation. Oxford University Press, Oxford, 280 pp.
doi: 10.1093/acprof:osobl/9780199587100.001.0001
Olson P.D., Littlewood D.T.J., Griffiths D., Kennedy C.R., Arme C. 2002: Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh, Northern Ireland. J. Helminthol. 76: 171.
pubmed: 12015830
doi: 10.1079/JOH2001101
Palm H.W., Theisen S., Pikalov E., Kleinertz S. 2018: An update: manipulation of fish phenotype by parasites. Ref. Mod. Life Sci. 2018: 1-9.
doi: 10.1016/B978-0-12-809633-8.20713-9
R Core Team 2021: R: a language and environment for statistical computing.
Ristau K., Steinfartz S., Traunspurger W. 2013: First evidence of cryptic species diversity and significant population structure in a widespread freshwater nematode morphospecies (Tobrilus gracilis). Mol. Ecol. 22: 4562-4575.
pubmed: 23927432
doi: 10.1111/mec.12414
Ronquist F., Huelsenbeck J.P. 2003: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
pubmed: 12912839
doi: 10.1093/bioinformatics/btg180
Rundle H.D., Nosil P. 2005: Ecological speciation. Ecol. Lett. 8: 336-352.
doi: 10.1111/j.1461-0248.2004.00715.x
Ryšavý B., Sitko J. 1995: New findings of tapeworms (Cestoda) of birds from Moravia and synopsis of bird Cestodes from Czech Republic. Acta Sci. Nat. Brno 29: 1-66.
Schirrmann M.K., Leuchtmann A. 2015: The role of host-specificity in the reproductive isolation of Epichloë endophytes revealed by reciprocal infections. Fungal Ecol. 15: 29-38.
doi: 10.1016/j.funeco.2015.02.004
Štefka J., Hypša V., Scholz T. 2009: Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Mol. Ecol. 18: 1187-1206.
pubmed: 19222754
doi: 10.1111/j.1365-294X.2008.04074.x
Stork N.E., Lyal C.H.C. 1993: Extinction or 'co-extinction' rates? Nature 366: 307.
doi: 10.1038/366307a0
Sweeting R.A. 1977: Studies on Ligula intestinalis. Some aspects of the pathology in the second intermediate host. J. Fish Biol. 10: 43-50.
doi: 10.1111/j.1095-8649.1977.tb04040.x
Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011: MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
doi: 10.1093/molbev/msr121
Van Dobben W.H. 1952: The food of the cormorant in the Netherlands. Ardea 55: 1-63.
doi: 10.5253/arde.v40.p1
Waeschenbach A., Brabec J., Scholz T., Littlewood D.T.J., Kuchta R. 2017: The catholic taste of broad tapeworms - multiple routes to human infection. Int. J. Parasitol. 47: 831-843.
doi: 10.1016/j.ijpara.2017.06.004
Wells K., Clark N.J. 2019: Host specificity in variable environments. Trends Parasitol. 35: 452-465.
pubmed: 31047808
doi: 10.1016/j.pt.2019.04.001
Windsor D.A. 1998: Controversies in parasitology. Most of the species on Earth are parasites. Int. J. Parasitol. 28: 1939-1941.
doi: 10.1016/S0020-7519(98)00153-2
Wyatt R.J., Kennedy C.R. 1989: Host-constrained epidemiology of the fish tapeworm Ligula intestinalis (L.). J. Fish Biol. 35: 215-227.
doi: 10.1111/j.1095-8649.1989.tb02971.x
Xia X., Lemey P. 2009: Assessing substitution saturation with DAMBE. In: P. Lemey, M. Salemi, A.-M. Vandamme (Eds.), The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny. Second Edition. Cambridge University Press, Cambridge, pp. 615-630.
doi: 10.1017/CBO9780511819049.022
Xia X., Xie Z. 2001: DAMBE: software package for data analysis in molecular biology and evolution. J. Hered. 92: 371-373.
doi: 10.1093/jhered/92.4.371
ZAR J.H. 1999: Biostatistical Analysis. Prentice Hall, New Jersey, 663 pp.