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Integrative taxonomy suggests that South American freshwater nematodes Echinocephalus and their host stingrays co-originated in late Oligocene to early Miocene

Published online by Cambridge University Press:  14 September 2022

M. I. Müller
Affiliation:
Department of Ecology and Evolutionary Biology, Federal University of São Paulo (Unifesp), Rua Arthur Riedel 275, Jd Eldorado, Diadema, SP CEP09972-270, Brazil
E. A. Adriano*
Affiliation:
Department of Ecology and Evolutionary Biology, Federal University of São Paulo (Unifesp), Rua Arthur Riedel 275, Jd Eldorado, Diadema, SP CEP09972-270, Brazil Department of Animal Biology, State University of Campinas (UNICAMP), Campinas, SP, Brazil
M. S.B. Oliveira
Affiliation:
Universidade Federal do Amapá. (UNIFAP), Programa de Pós-Graduação em Biodiversidade Tropical, Rodovia Juscelino Kubitschek, km2, Macapa, Amapa CEP68903-419, Brazil
L. L. Corrêa
Affiliation:
Universidade Federal do Oeste do Pará (UFOPA), Instituto de Ciências e Tecnologia das Águas (ICTA), Santarém, PA CEP68040-255, Brazil
*
Author for correspondence: E.A. Adriano, E-mail: adriano@unifesp.br

Abstract

Nematoda of the genus Echinocephalus Molin, 1858 include species from the Gnathostomatidae family, the adult stages of which parasitize the stomach and spiral intestine of elasmobranchs as their final hosts. In the present study, we describe Echinocephalus spinosus n. sp. found parasitizing the spiral valve of the freshwater stingray Potamotrygon motoro from the Tapajós River, in the Amazon Basin, in the state of Pará, Brazil. In the study we performed morphological (light and scanning electron microscopy) and molecular (small subunit ribosomal ribonucleic acid (SSU rDNA) and mitochondrial cytochrome c oxidase I sequencing) analyses. E. spinosus n. sp. is only the second species of the Echinocephalus genus described from a strictly freshwater environment. The SSU rDNA based phylogenetic analyses showed Echinocephalus clade as a sister lineage of Gnathostoma, and that the new species arises as a sister to Echinocephalus cf. pseudouncinatus. Time-calibrated phylogenetic analysis revealed that the origin of the freshwater Echinocephalus coincides with the recently proposed origin of the freshwater host potamotrygonin stingray, namely the late Oligocene to early Miocene, when the western Amazon was dominated by the Pebas wetlands, an epicontinental marine/freshwater system.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Abdel-Ghaffar, F, Bashtar, AR, Mehlhorn, H, Abdel-Gaber, R, Al Quraishy, S and Saleh, R (2013) Morphological and phylogenetic analysis of Echinocephalus carpiae n. sp. (Nematoda: Gnathostomatidae) infecting the common carp Cyprinus carpio inhabiting Burullus Lake—a new host record in Egypt. Parasitology Research 112(12), 40214028.CrossRefGoogle Scholar
Adnet, S, Salas Gismondi, R and Antoine, PO (2014) Comparisons of dental morphology in river stingrays (Chondrichthyes: Potamotrygonidae) with new fossils from the middle Eocene of Peruvian Amazonia rekindle debate on their evolution. Naturwissenschaften 101(1), 3345.CrossRefGoogle ScholarPubMed
Adriano, EA, Zatti, SA and Okamura, B (2021) How to build single-celled cnidarians with worm-like motility: lessons from Myxozoa. Journal of Anatomy 240(3), 475488.CrossRefGoogle ScholarPubMed
Bain, O, Mutafchiev, Y and Junker, K (2014) Order spirurida. 759 pp. In Schmidt-Rhaesa, A (Ed,) A handbook of zoology: Gastrotricha, cycloneuralia and gnathifera. Vol. 2 - Nematoda. Berlin/Boston, De Gruyter, .Google Scholar
Baylis, HA and Lane, C (1920) A revision of the nematode family Gnathostomidae. Proceedings of the Zoological Society of London 1920, 245310.CrossRefGoogle Scholar
Blasco-Costa, I, Faltynkova, A, Georgieva, S, Skrnisson, K, Scholz, T and Kostadinova, A (2014) Fish pathogens near the arctic circle: molecular, morphological and ecological evidence for unexpected diversity of Diplostomum (Digenea: Diplostomidae) in Iceland. International Journal for Parasitology 44(10), 703715.CrossRefGoogle Scholar
Bloom, DD and Lovejoy, NR (2017) On the origins of marine-derived freshwater fishes in South America. Journal of Biogeography 44(9), 19271938.CrossRefGoogle Scholar
Boeger, WA and Kritsky, DC (2003) Parasites, fossils and geologic history: historical biogeography of the south American freshwater croakers, Plagioscion spp. (Teleostei, Sciaenidae). Zoologica Scripta 32(1), 311.CrossRefGoogle Scholar
Bouckaert, R, Heled, J, Kühnert, D, Vaughan, T, Wu, CH, Xie, D, Suchard, M, Rambaut, A and Drummond, AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PloS Computational Biology 10(4), 16.CrossRefGoogle ScholarPubMed
Bray, DF, Bagu, J and Koegler, P (1993) Comparison of hexamethyldisilazane (HMDS), Peldri II, and critical-point drying methods for scanning electron microscopy of biological specimens. Microscopy Research and Technique 26(6), 489495.CrossRefGoogle Scholar
Brooks, DR and Deardorff, TL (1988) Rhinebothrium devaneyi n. sp. (Eucestoda: Tetraphyllidea) and Echinocephalus overstreeti Deardorff and Ko, 1983 (Nematoda: Gnathostomatidae) in a thorny back ray, Urogymnus asperrimus, from Enewetak Atoll, with phylogenetic analysis of both species groups. Journal of Parasitology 74(3), 459465.CrossRefGoogle Scholar
Carvalho, MR, Lovejoy, N and Rosa, R (2003) Family Potamotrygonidae (river stingrays). pp. 2228 in Reis, RE, Kullander, SO, and Ferraris, CJ Jr (Eds) Check list of the freshwater fishes of south and Central America. Porto Alegre/RS, EDIPUCRS.Google Scholar
Carvalho, MR, Maisey, JG and Grande, L (2004) Freshwater stingrays of the Green River Formation of Wyoming (early Eocene), with the description of a new genus and species and an analysis of its phylogenetic relationships (Chondrichthyes: Myliobatiformes). Bulletin of the American Museum of Natural History, 284(1), 1136.2.0.CO;2>CrossRefGoogle Scholar
Carvalho, MR, Loboda, TS and Silva, JPCB (2016) A new subfamily, Styracurinae and new genus, Styracura, for Himantura schmardae (Werner, 1904) and Himantura pacifica (Beebe & Tee-Van, 1941) (Chondrichthyes: Myliobatiformes). Zootaxa 4175(3), 201221.CrossRefGoogle Scholar
Cassens, I, Vicario, S, Waddell, VG, et al. (2000) Independent adaptation to riverine habitats allowed survival of ancient cetacean lineages. Proceedings of the National Academy of Sciences of the United States of America 97(21), 1134311347.CrossRefGoogle ScholarPubMed
Cavalcanti, MJ, Santos-Silva, EM and Primeiro, LJDOG (2019) Database of the marine-derived aquatic biota of the Amazon basin. Tropical Diversity 1(1), 1225.Google Scholar
Chabain, J, Antoine, PO, Altamirano-Sierra, AJ, Marivaux, L, Pujos, F, Gismondi, RS and Adnet, S (2017) Cenozoic batoids from Contamana (Peruvian Amazonia) with focus on freshwater potamotrygonins and their paleoenvironmental significance. Geobios 50(5–6), 389400.CrossRefGoogle Scholar
Dare, OK, Nadler, SA and Forbes, MR (2008) Nematode lungworms of two species of anuran amphibians: evidence for co-adaptation. International Journal for Parasitology 38(14), 17291736.CrossRefGoogle ScholarPubMed
Deardorff, TL, Brooks, DR and Thorson, TB (1981) A new species of Echinocephalus (Nematoda: Gnathostomatidae) from neotropical stingrays with comments on E. diazi. Journal of Parasitology 67(3), 433439.CrossRefGoogle Scholar
Drummond, AJ, Ho, SYW, Phillips, MJ and Rambaut, A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology 4(5), 699710.CrossRefGoogle Scholar
Dubey, S and Shine, R (2008) Origin of the parasites of an invading species, the Australian cane toad (Bufo marinus): are the lungworms Australian or American? Molecular Ecology 17(20), 44184424.CrossRefGoogle ScholarPubMed
Dunn, IS and Blattner, FR (1987) Charons 36-40: multi enzyme, high capacity, recombination deficient replacement vectors with polylinkers and polystuffers. Nucleic Acids Research 15(6), 26772698.CrossRefGoogle ScholarPubMed
Edgar, RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5(1), 113.CrossRefGoogle ScholarPubMed
Floyd, RM, Rogers, AD, Lambshead, PJD and Smith, CR (2005) Nematode-specific PCR primers for the 18S small subunit rRNA gene. Molecular Ecology Notes 5(3), 611612.CrossRefGoogle Scholar
Folmer, O, Black, MB, Wr, H, Lutz, R and Vrijenhoek, RC (1994) DNA primers for amplification of mitochondrial C oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3(5), 294299.Google ScholarPubMed
Fontenelle, JP, Marques, FPL, Kolmann, MA and Lovejoy, NR (2021) Biogeography of the neotropical freshwater stingrays (Myliobatiformes: Potamotrygoninae) reveals effects of continent-scale paleogeographic change and drainage evolution. Journal of Biogeography 48(6), 14061419.CrossRefGoogle Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52(5), 696704.CrossRefGoogle ScholarPubMed
Hamilton, H, Caballero, S, Collins, AG and Brownell, RL Jr (2001) Evolution of river dolphins. Proceedings of the Royal Society of London. Series B: Biological Sciences 268(1466), 549556.CrossRefGoogle ScholarPubMed
Hugot, JP, Gardner, SL, Borba, V, Araujo, P, Leles, D, Rosa, AAS, Dutra, J, Ferreira, LF and Araujo, A (2014) Discovery of a 240 million year old nematode parasite egg in a cynodont coprolite sheds light on the early origin of pinworms in vertebrates. Parasites & Vectors 7(1), 486.Google Scholar
Karagiorchis, C, Ploeg, RJ, Ghafar, A, et al. (2022) Genetic characterisation of Echinocephalus spp. (Nematoda: Gnathostomidae) from marine hosts in Australia. International Journal for Parasitology: Parasite and Wildlife 17(1), 161167.Google Scholar
Kearse, M, Moir, R, Wilson, A, et al. (2012) Geneious Basic: an integrated and extendable desktop software plat- form for the organization and analysis of sequence data. Bioinformatics 28(12), 16471649.CrossRefGoogle Scholar
Kimura, M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16(2), 111120.CrossRefGoogle ScholarPubMed
Kirchhoff, KN, Hauffe, T, Stelbrink, B, Albrecht, C and Wilke, T (2017) Evolutionary bottlenecks in brackish water habitats drive the colonization of fresh water by stingrays. Journal of Evolutionary Biology 30(8), 15761591.CrossRefGoogle ScholarPubMed
Lacerda, ACF, Takemoto, RM and Pavanelli, GC (2009) Ecology of endoparasites of the fluvial stingray Potamotrygon falkneri (Chondrichthyes: Potamotrygonidae) from the upper Paraná River floodplain, Brazil. Brazilian Journal of Biology 69(2), 297303.CrossRefGoogle ScholarPubMed
Laetsch, DR, Heitlinger, EG, Taraschewski, H, Nadler, SA and Blaxter, ML (2012) The phylogenetics of Anguillicolidae (Nematoda: Anguillicolidea), swimbladder parasites of eels. BMC Evolutionary Biology 12(1), 60.CrossRefGoogle Scholar
Langford, GJ and Janovy, J Jr (2013) Host specificity of North American Rhabdias spp. (Nematoda: Rhabdiasidae): Combining field data and experimental infections with a molecular phylogeny. Journal of Parasitology 99(2), 277286.CrossRefGoogle ScholarPubMed
Laval, BE, Imberger, J and Findikakis, AN (2005) Dynamics of a large tropical lake: Lake Maracaibo. Aquatic Science 67(3), 337349.CrossRefGoogle Scholar
Levêque, C, Oberdorff, T, Paugy, D, Stiassny, MLJ and Tedesco, PA (2008) Global diversity of fish (Pisces) in freshwater. Hydrobiologia 595(1), 545567.CrossRefGoogle Scholar
Loboda, TS, Lasso, CA, Rosa, RS and Carvalho, MR (2021) Two new species of freshwater stingrays of the genus Paratrygon (Chondrichthyes: Potamotrygonidae) from the Orinoco basin, with comments on the taxonomy of Paratrygon aiereba. Neotropical Ichthyology 19(2), e200083.CrossRefGoogle Scholar
Lovejoy, NR, Bermingham, E and Martin, AP (1998) Marine incursion into South America. Nature 396(6710), 421422.CrossRefGoogle Scholar
Lovejoy, NR, Albert, JS and Crampton, WGR (2006) Miocene marine incursions and marine/freshwater transitions: evidence from Neotropical fishes. Journal of South American Earth Sciences 21(1– 2), 513.CrossRefGoogle Scholar
Lundberg, JG, Marshall, LG, Guerrero, J, Horton, B, Malabarba, MCSL and Wesselingh, F (1998) The stage for Neotropical fish diversification: a history of tropical South American rivers. p. 603 in Malabarba MCSL, Reis RE, Vari RP, Lucena ZM and Lucena CAS (Eds). Phylogeny and classification of neotropical Fishes. Part 1 - Fossils and Geological Evidence. Porto Alegre: Edipucrs.Google Scholar
Moravec, F and Justine, JL (2021) Echinocephalus inserratus sp. n. (Nematoda: Gnathostomidae) from the stingray Pastinachus ater (Dasyatidae) and new records of congeneric and some other nematode larvae from teleost fishes off New Caledonia. Folia Parasitologica 68, 2021.014.CrossRefGoogle Scholar
Nadler, SA, Carreno, RA, Mejia-Madrid, H, Ullberg, J, Pagan, C, Houston, R and Hugot, JP (2007) Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology 134(10), 14211442.CrossRefGoogle ScholarPubMed
Nelson, JS, Grande, TC and Wilson, MVH (2016) Fishes of the world. 5th ed. Hoboken, New Jersey, John Wiley & Sons.CrossRefGoogle Scholar
Nuttall, C (1990) A review of the tertiary non-marine molluscan faunas of the Pabasian and other inland basins of north-Western South America. Bulletin of the British Museum Natural History (Geology) 45(2), 165372.Google Scholar
Oliveira, MSB, Corrêa, LL, Adriano, EA and Tavares-Dias, M (2021) Integrative taxonomy of a new species of Therodamas (Ergasilidae) infecting the Amazonian freshwater fish Leporinus fasciatus (Anostomidae). Parasitology Research 120(9), 31373147.CrossRefGoogle Scholar
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48(1), 369371.CrossRefGoogle Scholar
Posada, D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25(7), 12531256.CrossRefGoogle ScholarPubMed
Rambaut, A (2009) Molecular evolution, phylogenetics and epidemiology: Fig-Tree, Available at http//tree.bio.ed.ac.uk/software/figtree/ (Accessed 10 May 2021).Google Scholar
Rambaut, A (2020) Molecular evolution, phylogenetics and epidemiology: Fig-Tree. Available at http://tree.bio.ed.ac.uk/software/fgtree/ (accessed 10 December 2021).Google Scholar
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67(5), 901904.CrossRefGoogle ScholarPubMed
Räsänen, ME, Linna, AM, Santos, JCR and Negri, FR (1995) Late Miocene tidal deposits in the Amazonian foreland basin. Science 269(5222), 386390.CrossRefGoogle ScholarPubMed
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12), 15721574.CrossRefGoogle ScholarPubMed
Saad, CB, Suthar, J, Theisen, S, Palm, HW and Gargouri, L (2022) Echinocephalus caniculus n. sp. (Nematoda: Gnathostomidae Railliet, 1985) from the lesser spotted dogfish Scyliorhinus canicula (L.) (Elasmobranchii: Scyliorhinidae Gill 1862) off Tunisia, with a key to species of the genus Echinocephalus. Systematic Parasitology 99(3), 299307.CrossRefGoogle Scholar
Silva, JPCB and Loboda, TS (2019) Potamotrygon marquesi, a new species of neotropical freshwater stingray (Potamotrygonidae) from the Brazilian Amazon Basin. Journal of Fish Biology 95(2), 594612.CrossRefGoogle Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30(12), 27252729.CrossRefGoogle ScholarPubMed
Troncy, PM (1970) Description de deux nouvelles espèces de nématodes parasites de poissons [Description of two new species of fish parasitic nematodes]. Bulletin du Muséum d'Histoire Naturelle 41(2), 598605. [In French.]Google Scholar
Van Megen, H, Van den Elsen, S, Holterman, M, Karssen, G, Mooyman, P, Bongers, T, Holovachov, O, Bakker, J and Helder, J (2009) A phylogenetic tree of nematodes based on about 1200 full-length small subunit ribosomal DNA sequences. Nematology 11(6), 927950.CrossRefGoogle Scholar
Ward, RD, Zemlak, TS, Innes, BH, Last, PR and Hebert, PDN (2005) DNA barcoding Australia`s fish species. Philosophical Transactions of the Royal Society B 360(1462), 18471857.CrossRefGoogle ScholarPubMed
Xia, X (2013) DAMBE. A comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution 30(7), 17201728.CrossRefGoogle ScholarPubMed
Zatti, SA, Adriano, EA, Araújo, BL, Franzolin, GN and Maia, AAM (2022) Expanding the geographic distribution of the freshwater parasite Ceratomyxa (Cnidaria: Myxozoa) with vermiform-type plasmodia. Microbiology Pathogenesis 162(1), 16.CrossRefGoogle ScholarPubMed
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