Uncharted digenean diversity in Lake Tanganyika: cryptogonimids (Digenea: Cryptogonimidae) infecting endemic lates perches (Actinopterygii: Latidae)

. 2020 May 01 ; 13 (1) : 221. [epub] 20200501

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32357898

Grantová podpora
P505/12/G112 Grantová Agentura České Republiky
GA19-13573S Grantová Agentura České Republiky
GOH3817N Fonds Wetenschappelijk Onderzoek
8J18AT007 Ministerstvo Školství, Mládeže a Tělovýchovy
NDOC2016PR006 Directorate-General for International Cooperation and Development
FJCI-2016-29535 Ministerio de Ciencia e Innovación
MUNI/A/0918/2018 Masarykova Univerzita

Odkazy

PubMed 32357898
PubMed Central PMC7195733
DOI 10.1186/s13071-020-3913-x
PII: 10.1186/s13071-020-3913-x
Knihovny.cz E-zdroje

BACKGROUND: Lake Tanganyika is considered a biodiversity hotspot with exceptional species richness and level of endemism. Given the global importance of the lake in the field of evolutionary biology, the understudied status of its parasite fauna is surprising with a single digenean species reported to date. Although the most famous group within the lake's fish fauna are cichlids, the pelagic zone is occupied mainly by endemic species of clupeids (Actinopterygii: Clupeidae) and lates perches (Actinopterygii: Latidae, Lates Cuvier), which are an important commercial source for local fisheries. In this study, we focused on the lake's four lates perches and targeted their thus far unexplored endoparasitic digenean fauna. METHODS: A total of 85 lates perches from four localities in Lake Tanganyika were examined. Cryptogonimid digeneans were studied by means of morphological and molecular characterisation. Partial sequences of the nuclear 28S rRNA gene and the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene were sequenced for a representative subset of the specimens recovered. Phylogenetic analyses were conducted at the family level under Bayesian inference. RESULTS: Our integrative approach revealed the presence of six species within the family Cryptogonimidae Ward, 1917. Three out of the four species of Lates were found to be infected with at least one cryptogonimid species. Two out of the three reported genera are new to science. Low interspecific but high intraspecific phenotypic and genetic diversity was found among Neocladocystis spp. Phylogenetic inference based on partial 28S rDNA sequences revealed a sister group relationship for two of the newly erected genera and their close relatedness to the widely distributed genus Acanthostomum Looss, 1899. CONCLUSIONS: The present study provides the first comprehensive characterisation of the digenean diversity in a fish family from Lake Tanganyika which will serve as a baseline for future explorations of the lake's digenean fauna. Our study highlights the importance of employing an integrative approach for revealing the diversity in this unique host-parasite system.

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Cohen AS, Soreghan MJ, Scholz CA. Estimating the age of formation of lakes: an example from Lake Tanganyika, East African Rift system. Geology. 1993;21:511–514.

Nishida M. Lake Tanganyika as an evolutionary reservoir of old lineages of East African cichlid fishes: inferences from allozyme data. Experientia. 1991;47:974–979.

Wilson AB, Glaubrecht M, Meyer A. Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika. Proc R Soc London Ser B Biol Sci. 2004;271:529–536. PubMed PMC

Snoeks J. Ancient lakes: biodiversity, ecology and evolution. Adv Ecol Res. 2000;31:17–38.

Salzburger W, Van Bocxlaer B, Cohen AS. Ecology and evolution of the African Great Lakes and their faunas. Annu Rev Ecol Evol Syst. 2014;45:519–545.

Vanhove MPM, Pariselle A, Van Steenberge M, Raeymaekers JAM, Hablützel PI, Gillardin C, et al. Hidden biodiversity in an ancient lake: phylogenetic congruence between Lake Tanganyika tropheine cichlids and their monogenean flatworm parasites. Sci Rep. 2015;5:13669. PubMed PMC

Coulter GW. Composition of the flora and fauna. In: Coulter GW, editor. Lake Tanganyika and its life. Oxford: Oxford University Press; 1991. pp. 200–274.

Kuchta R, Basson L, Cook C, Fiala I, Bartošová-Sojková P, Řehulková E. A systematic survey of the parasites of freshwater fishes in Africa. In: Scholz T, Vanhove MPM, Jayasundera Z, Gelnar M, editors. A guide to the parasites of African freshwater fishes. Brussels: Abc Taxa; 2018. pp. 135–360.

Pariselle A, Van Steenberge M, Snoeks J, Volckaert FAM, Huyse T, Vanhove MPM. Ancyrocephalidae (Monogenea) of Lake Tanganyika: does the Cichlidogyrus parasite fauna of Interochromis loocki (Teleostei, Cichlidae) reflect its host’s phylogenetic affinities? Contrib Zool. 2015;84:25–38.

Pariselle A, Muterezi Bukinga F, Van Steenberge M, Vanhove MPM. Ancyrocephalidae (Monogenea) of Lake Tanganyika: IV: Cichlidogyrus parasitizing species of Bathybatini (Teleostei, Cichlidae): reduced host-specificity in the deepwater realm? Hydrobiologia. 2015;748:99–119.

Kmentová N, Gelnar M, Mendlová M, Van Steenberge M, Koblmüller S, Vanhove MPM. Reduced host-specificity in a parasite infecting non-littoral Lake Tanganyika cichlids evidenced by intraspecific morphological and genetic diversity. Sci Rep. 2016;6:39605. PubMed PMC

Kmentová N, Van Steenberge M, Raeymaekers JAR, Koblmüller S, Hablützel PI, Muterezi Bukinga F, et al. Monogenean parasites of sardines in Lake Tanganyika: diversity, origin and intra-specific variability. Contrib Zool. 2018;87:105–132.

Rahmouni C, Vanhove MPM, Šimková A. Underexplored diversity of gill monogeneans in cichlids from Lake Tanganyika: eight new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) from the northern basin of the lake, with remarks on the vagina and the heel of the male copu. Parasit Vectors. 2017;10:591. PubMed PMC

Rahmouni C, Vanhove MPM, Šimková A. Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) parasitizing the gills of Congolese cichlids from northern Lake Tanganyika. PeerJ. 2018;6:e5604. PubMed PMC

Baylis HA. Some parasitic worms, mainly from fishes, from Lake Tanganyika. Ann Mag Nat Hist. 1928;1:552–562.

Kmentová N, Koblmüller S, Van Steenberge M, Artois T, Bukinga FM, N‘sibula TM, et al. Failure to diverge in African Great Lakes: the case of Dolicirroplectanum lacustre comb. nov. (Monogenea, Diplectanidae) infecting latid hosts. J Great Lakes Res. 2019 doi: 10.1016/j.jglr.2019.09.022. DOI

Coulter GW. The biology of Lates species (Nile perch) in Lake Tanganyika, and the status of the pelagic fishery for Lates species and Luciolates stappersii (Blgr.) J Fish Biol. 1976;9:235–259.

Plisnier PD, Mgana H, Kimirei I, Chande A, Makasa L, Chimanga J, et al. Limnological variability and pelagic fish abundance (Stolothrissa tanganicae and Lates stappersii) in Lake Tanganyika. Hydrobiologia. 2009;625:117–134.

Lowe-McConnell RH. Fish faunas of the African Great Lakes: origins, diversity, and vulnerability. Conserv Biol. 1993;7:634–643.

Coulter GW. Pelagic Fish. In: Coulter GW, editor. Lake Tanganyika and its life. Oxford: Oxford University Press; 1991. pp. 111–150.

Koblmüller S, Odhiambo EA, Sinyinza D, Sturmbauer C, Sefc KM. Big fish, little divergence: phylogeography of Lake Tanganyika’s giant cichlid, Boulengerochromis microlepis. Hydrobiologia. 2015;748:29–38. PubMed PMC

De Keyzer ELR, De Corte Z, Van Steenberge M, Raeymaekers JAM, Calboli FCF, Kmentová N, et al. First genomic study on Lake Tanganyika sprat Stolothrissa tanganicae: a lack of population structure calls for integrated management of this important fisheries target species. BMC Evol Biol. 2019;19:6. PubMed PMC

Koblmüller S, Zangl L, Börger C, Daill D, Vanhove MPM, Sturmbauer C, et al. Only true pelagics mix: comparative phylogeography of deepwater bathybatine cichlids from Lake Tanganyika. Hydrobiologia. 2019;832:93–103. PubMed PMC

Emere MC. Parasitic Infection of the Nile Perch Lates niloticus (L) in River Kaduna. J Aquat Sci. 2000;15:51–54.

Issa GI. Description of Acanthostomum niloticum n. sp. and Acanthostomum spiniceps knobus n. subsp. (Trematoda, Acanthostomidae) from the river Nile, Egypt. Wildl Dis Assoc. 1980;31:1962.

Brooks DR. Revision of the Acanthostominae Poche, 1926 (Digenea: Cryptogonimidae) Zool J Linn Soc. 1980;70:313–382.

Abdel-Gaber R, Abdel-Ghaffar F, Mehlhorn H, Al Quraishy S, Morsy K, Maher S. Light microscopic study of four plagiorchiid trematodes infecting marine fish in the south-eastern Mediterranean Sea, Alexandria City, with descriptions of two new species. Parasitol Res. 2018;117:1341–1356. PubMed

Hamouda AH, Sorour SS, El-habashi NM, Adam EA. Parasitic infection with emphasis on Tylodelphys spp. as new host and locality records in Nile perch; Lates niloticus from Lake Nasser, Egypt. World Vet J. 2018;8:19–33.

Klapper R, Meyer C, Kuhn T, Karl H. Food safety aspects of fresh Nile perch (Lates niloticus) fillets from Lake Victoria imported to the European market: helminth parasites and microbiological status. Food Control. 2017;78:311–316.

Bray RA, Cribb TH. Species of Stephanostomum Looss, 1899 (Digenea: Acanthocolpidae) from fishes of Australian and South Pacific waters, including five new species. Syst Parasitol. 2003;55:159–197. PubMed

Chatterji PN. On a new species of the genus Psilostomum Looss, 1899. Indian J Helminthol. 1958;8:96–99.

Smith JW. The blood flukes (Digenea: Sanguinicolidae and Spirorchidae) of cold-blooded vertebrates and some comparison with the schistosomes. Helminthol Abst. 1972;41:161–204.

Herbert BW, Shaharom FM. A new blood fluke, Parasanguinicola vastispina gen. nov., sp. nov. (Trematoda: Sanguinicolidae), from sea bass, Lates calcarifer (Centropomidae) cultured in Malaysia. Parasitol Res. 1995;81:349–354. PubMed

Arthur JR, Lumanlan-Mayo S. Checklist of the parasites of fishes of the Philippines. Rome: FAO Fisheries Technical Paper; 1997.

Rückert S, Palm HW, Klimpel S. Parasite fauna of seabass (Lates calcarifer) under mariculture conditions in Lampung Bay, Indonesia. J Appl Ichthyol. 2008;24:321–327.

Bilqees FM. Teaching and research in marine parasitology - problems and solution. Proc Parasitol. 1995;20:63–89.

Bilqees FM. A new trematode genus Pseudohypertrema from fishes of the Karachi coast Pakistan. Nor J Zool. 1976;24:201–203.

Bray RA, Cribb TH, Barker SC. Hemiuridae (Digenea) from marine fishes of the Great Barrier Reef, Queensland, Australia. Syst Parasitol. 1993;25:37–62.

Yamaguti S. Parasitic worms mainly from Celebes. Part 1. New digenetic trematodes of fishes. Acta Med Okayama. 1952;8:146–198.

Rodgers LJ, Burke JB. Aetiology of “red spot” disease (vibriosis) with special reference to the ectoparasitic digenean Prototransversotrema steeri (Angel) and the sea mullet, Mugil cephalus (Linnaeus) J Fish Biol. 1988;32:655–663.

Cribb T, Bray R, Barker S. A review of the family Transversotrematidae (Trematoda : Digenea) with the description of a new genus, Crusziella. Invertebr Syst. 1992;6:909.

Bray RA, Cribb TH. Ningalooia psammopercae n. g., n. sp. (Digenea: Acanthocolpidae) from the Waigieu seaperch Psammoperca waigiensis (Cuvier) (Perciformes: Latidae) on the Ningaloo Reef, Western Australia. Syst Parasitol. 2007;66:131–135. PubMed

Prudhoe S. Trematoda, Cestoda and Acanthocephala. Résultats Sci l’Exploration Hydrobiol du Lac Tanganika. 1951;3:1–10.

Miller TL, Cribb TH. Family Cryptogonimidae Ward, 1917. In: Bray RA, Gibson DI, Jones A, editors. Keys to the Trematoda. Wallingford-London: CAB International and Natural History Museum; 2008. pp. 51–112.

Looss A. Ueber die Fasciolidengenera Stephanochasmus, Acanthochasmus und einige andere. Centrbl Bak. 1901;29:595–661.

Dollfus RP. Trematodes récolths au Congo Belge par le Professeur Paul Brien (mai-août 1937) Ann Mus Congo Beig. 1950;1:1–135.

Fischthal JH, Thomas JD. Digenetic trematodes of some freshwater and marine fishes from Ghana. Proc Helminthol Soc Wash. 1968;35:126–140.

Manter HW, Pritchard MH. Some digenetic trematodes of Central Africa chiefly from fishes. Rev Zool Bot Afr. 1969;80:51–61.

Moravec F. On two acanthostomatid trematodes, Acanthostomum spiniceps (Looss, 1896) and A. absconditum (Looss, 1901), from African bagrid fishes. Folia Parasitol (Praha) 1976;23:201–206. PubMed

Marcogliese DJ. Parasites of the superorganism: are they indicators of ecosystem health? Int J Parasitol. 2005;35:705–716. PubMed

Danley PD, Husemann M, Ding B, Dipietro LM, Beverly EJ, Peppe DJ. The impact of the geologic history and paleoclimate on the diversification of East African cichlids. Int J Evol Biol. 2012;2012:574851. PubMed PMC

Ergens R, Lom J. Causative agents of fish diseases. Prague: Academia; 1970.

Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, et al. Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol Phylogenet Evol. 2008;48:369–371. PubMed

ICZN International Commission on Zoological Nomenclature: Amendment of articles 8, 9, 10, 21 and 78 of the International Code of Zoological Nomenclature to expand and refine methods of publication. Bull Zool Nomencl. 2012;69:161–169. PubMed

Dallarés S, Georgieva S, Kostadinova A, Carrassón M, Gibson DI, Pérez-del-Olmo A. Morphometric and molecular characterisation of specimens of Lepidapedon Stafford, 1904 (Digenea: Lepidapedidae) from the deep-sea fish Mora moro (Risso) (Teleostei: Moridae) in the western Mediterranean. Syst Parasitol. 2013;85:243–253. PubMed

Tkach VV, Littlewood DTJ, Olson PD, Kinsella JM, Swiderski Z. Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea) Syst Parasitol. 2003;56:1–15. PubMed

Bowles J, Blair D, McManus DP. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol. 1992;54:165–173. PubMed

Miura O, Kuris AM, Torchin ME, Hechinger RF, Dunham EJ, Chiba S. Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse) Int J Parasitol. 2005;35:793–801. PubMed

Littlewood DTJ, Curini-Galletti M, Herniou EA. The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol Phylogenet Evol. 2000;16:449–466. PubMed

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. PubMed PMC

Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol. 2013;30:772–780. PubMed PMC

Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–552. PubMed

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;27:221–224. PubMed

Kumar S, Stecher G, Tamura K, Gerken J, Pruesse E, Quast C, et al. MEGA7: Molecular Evolutionary Genetics Analysis version 70 for bigger datasets. Mol Biol Evol. 2016;33:1870–1874. PubMed PMC

Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772. PubMed PMC

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539–542. PubMed PMC

Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop. IEEE Xplore; 2010. p. 1–8

Rambaut A, Suchard MA, Drummond AJ. Tracer v1.6; 2014. http://beast.community. Accessed 15 Apr 2019.

Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda) Int J Parasitol. 2003;33:733–755. PubMed

Khalil LF, Thurston JP. Studies on the helminth parasites of freshwater fishes of Uganda including the descriptions of two new species of digeneans. Rev Zool Bot Afr. 1973;87:209–248.

Vaz Z. Contribuiçao ao conhecimento dos Trematoides de peixes fluviaes do Brasil. Ina Diss (Doctoral thesis), Institute of Biology, Sao Paulo; 1932.

Quintana MG, Ostrowski de Núñez M. The life cycle of Neocladocystis intestinalis (Vaz, 1932) (Digenea: Cryptogonimidae), in Aylacostoma chloroticum (Prosobranchia: Thiaridae), and Salminus brasiliensis (Characiformes: Characidae), in Argentina. Parasitol Res. 1932;2016(115):2589–2595. PubMed

Miller TL, Cribb TH. Dramatic phenotypic plasticity within species of Siphomutabilus n.g. (Digenea: Cryptogonimidae) from Indo-Pacific caesionines (Perciformes: Lutjanidae) Syst Parasitol. 2013;86:101–112. PubMed

Hassanine RME, Gibson DI. Trematodes of Red Sea fishes: Hexangium brayi n. sp. (Angiodictyidae Looss, 1902) and Siphodera aegyptensis n. sp. (Cryptogonimidae Ward, 1917), with a review of their genera. Syst Parasitol. 2005;61:215–222. PubMed

Machida M. Monorchiidae (Trematoda, Digenea) from fishes of Japanese and adjacent waters. Bull Natl Sci Mus Tokyo Ser A Zool. 2005;31:123–136.

Miller TL, Cribb TH. Coevolution of Retrovarium n. gen. (Digenea: Cryptogonimidae) in Lutjanidae and Haemulidae (Perciformes) in the Indo-West Pacific. Int J Parasitol. 2007;37:1023–1045. PubMed

Miller TL, Adlard RD, Bray RA, Justine JL, Cribb TH. Cryptic species of Euryakaina n. g. (Digenea: Cryptogonimidae) from sympatric lutjanids in the Indo-West Pacific. Syst Parasitol. 2010;77:185–204. PubMed

Sefc K, Mattersdorfe K, Ziegelbecker A, Neuhüttler N, Steiner O, Goessler W, et al. Shifting barriers and phenotypic diversification by hybridization. Ecol Lett. 2017;20:651–662. PubMed PMC

Fryer G. Evolution in ancient lakes: radiation of Tanganyikan atyid prawns and speciation of pelagic cichlid fishes in Lake Malawi. Hydrobiologia. 2006;568:131–142.

Meixner MJ, Lüter C, Eckert C, Itskovich V, Janussen D, von Rintelen T, et al. Phylogenetic analysis of freshwater sponges provide evidence for endemism and radiation in ancient lakes. Mol Phylogenet Evol. 2007;45:875–886. PubMed

Glaubrecht M. Adaptive radiation of thalassoid gastropods in Lake Tanganyika, East Africa: morphology and systematization of a paludomid species flock in an ancient lake. Zoosyst Evol. 2008;84:71–122.

Hecky RE. The pelagic ecosystem. In: Coulter GW, editor. Lake Tanganyika and its life. Oxford: Oxford University Press; 1991. pp. 91–110.

Rohde K, Hayward C, Heap M. Aspects of the ecology of metazoan ectoparasites of marine fishes. Int J Parasitol. 1995;25:945–970. PubMed

Luque JL, Mouillot D, Poulin R. Parasite biodiversity and its determinants in coastal marine teleost fishes of Brazil. Parasitology. 2004;128:671–682. PubMed

Klimpel S, Palm HW, Busch MW, Kellermanns E, Rückert S. Fish parasites in the Arctic deep-sea: poor diversity in pelagic fish species vs. heavy parasite load in a demersal fish. Deep Sea Res Part I Oceanogr Res Pap. 2006;53:1167–1181.

Mölsä H, Reynolds JE, Coenen EJ, Lindqvist OV. Fisheries research towards resource management on Lake Tanganyika. Hydrobiologia. 1999;407:1–24.

Mannini P, Katonda I, Kissaka B, Verburg P. Feeding ecology of Lates stappersii in Lake Tanganyika. Hydrobiologia. 1999;407:131–139.

Miller T, Cribb T. Eight new species of Siphoderina Manter, 1934 (Digenea, Cryptogonimidae) infecting Lutjanidae and Haemulidae (Perciformes) off Australia. Acta Parasitol. 2008;53:344–364.

Miller TL, Cutmore SC, Cribb TH. Two species of Neometadena Hafeezullah & Siddiqi, 1970 (Digenea: Cryptogonimidae) from Moreton Bay, Australia, including the description of Neometadena paucispina n. sp. from Australian Lutjanidae. Syst Parasitol. 2018;95:655–664. PubMed

Poulin R. Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. J Fish Biol. 2000;56:123–137.

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