Abstract
In South America, the family Philometridae is represented by several genera and species. In particular, Philometra and Philometroides are the most speciose genera. In Argentina, only Philometroides tahieli has been reported so far. The main objective of this study was to analyze the phylogenetic relationship between Ps. tahieli and other South American philometrids using molecular data. The molecular analysis was performed using a female specimen of Ps. tahieli found on the opercular muscle of a juvenile Micropogonias furnieri from brackish waters in Argentina. Phylogenetic relationships were studied based on partial sequences of the 18S rDNA and 28S rDNA genes. In the 18S rDNA tree, Ps. tahieli was mainly grouped with other Philometroides from freshwater hosts from China, sharing the site of infection (head tissues or muscles). In the 28S rDNA tree, obtained with fewer sequences, Ps. tahieli is related species from subcutaneous tissues of head. This study contributes with information on philometrids and confirms the presence of different lineages among South American species, with Ps. tahieli representing a new one. Further studies on South American species using more molecular markers and new morphological characters will improve our knowledge of philometrid biodiversity and phylogeny.
Similar content being viewed by others
Data availability
All the material will be deposited in museums, and sequences will be deposited on GenBank.
Code availability
Not applicable.
References
Abe N, Aono S, Baba T (2019) Site of infection and genetic analysis of Philometroides branchiostegi-like nematode found in horsehead tilefish Branchiostegus japonicus. Nippon Suisan Gakkaishi 85:64–66. https://doi.org/10.2331/suisan.18-00023
Barton DP, Moravec F, Zhu X, Shamsi S (2022) Phylogenetic relationships of philometrid nematodes (Philometridae Baylis and Daubney, 1926) inferred from 18S rRNA, with molecular characterisation of recently described species Parasitol Res https://doi.org/10.1007/s00436-021-07373-8
Cárdenas MQ, Moravec F, Fernandes BMM, Morais AM (2012) A new species of Philometra Costa, 1845 (Nematoda: Philometridae) from the freshwater fish (red piranha) Pygocentrus nattereri Kner (Characidae) in Amazonia. Brazil Syst Parasitol 83(2):137–144
Cárdenas MQ, Moravec F, Kohn A (2009) First record of Philometra katsuwoni (Nematoda, Philometridae), a parasite of skipjack tuna Katsuwonus pelamis (Perciformes, Scombridae), off South American Atlantic Coast Biota Neotrop. https://doi.org/10.1590/S1676-06032009000200025
Cavalcante PHO, Moravec F, Santos CP (2017) The philometrid nematode Philometroides acreanensis n. sp. from the stomach wall of the catfsh Pimelodus blochii in North-Western Brazil. J Helmint. https://doi.org/10.1017/S0022149X1700013X
Černotíková E, Horák A, Moravec F (2011). Phylogenetic relationships of some spirurine nematodes (Nematoda: Chromadorea: Rhabditida: Spirurina) parasitic in fishes inferred from SSU rRNA gene sequences. Folia Parasitol. https://doi.org/10.14411/fp.2011.013.
Crisp DJ, Klein VLM (1973) Contribution to the knowledge of Philometra lateolabracis Yamaguti, 1935 (Nematoda, Filarioidea). Mem Inst Oswaldo Cruz 71(4):481–484
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v6.0.5 Available from http://www.geneious.com/ Accessed March 2020.
Genc E, Keskin E (2012) Philometra lateolabracis Steindachner, 1878 (Nematoda: Philometridae) in Epinephelus costae (Osteichthyes, Serranidae): first molecular identification of the histozoic parasite from Iskenderun Bay, northeast Mediterranean. In: AQUA 2012 Meeting Abstract. Wold Aquaculture Society Meetings, Prague, p 695
Iannacone J (2003). Tres metazoos parásitos de la cojinoba Seriolella violacea Guichenot (Pisces, Centrolophidae), Callao, Perú. Rev Bras Zool. https://doi.org/10.1590/S0101-81752003000200014.
Iwaki T, Tamai K, Ohimoto K, Iwahashi Y, Waki T, Kawano F, Ogawa K (2020) New records of Philometra pellucida (Jägerskiöld, 1893) (Nematoda: Philometridae) from the body cavity of Arothron mappa (Lesson) and Arothron nigropunctatus (Bloch et Schneider) reared in aquariums, with synonymisation of Philometra robusta Moravec, Möller et Heeger, 1992. Folia Parasitol. https://doi.org/10.14411/fp.2020.025
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization Brief Bioinform https://doi.org/10.1093/bib/bbx108
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) Mega X: molecular evolutionary genetics analysis across computing platforms Mol Biol Evol https://doi.org/10.1093/molbev/msy096
Lanfear R, Calcott B, Kainer D, Mayer C, Stamatakis A (2014) Selecting optimal partitioning schemes for phylogenomic datasets BMC Evol Biol https://doi.org/10.1186/1471-2148-14-82
Montes MM, Plaul SE, Martorelli SR (2016). A new species of philometrid parasite (Nematoda, Philometridae) and histopathological lesions in juvenile croakers, Micropogonias furnieri (Desmarest). J Fish Dis. https://doi.org/10.1111/jfd.12439.
Moravec F (2006) Dracunculoid and Anguillicoloid nematodes parasitic in vertebrates, 1st edn. Academia, Prague
Moravec F (2007) Some aspects of the taxonomy and biology of adult spirurine nematodes parasitic in fishes: a review. Folia Parasitol 54:239–257
Moravec F (2013). Some aspects of the taxonomy and biology of adult spirurine nematodes parasitic in fishes: a review. Folia Parasitol. https://doi.org/10.14411/fp.2007.033.
Moravec F, Chávez RA, Oliva ME (2011) A new gonad-infecting species of Philometra (Nematoda: Philometridae) from the red cusk-eel Genypterus chilensis (Osteichthyes: Ophidiidae) off Chile. Parasitol Res 108:227–232. https://doi.org/10.1007/s00436-010-2054-0
Moravec F, Ali A, Abed J, Shaker S (2016) New records of philometrids (Nematoda: Philometridae) from marine fishes off Iraq, with the erection of two new species and the first description of the male of Philometroides eleutheronemae Moravec and Manoharan, 2013. Syst Parasitol. https://doi.org/10.1007/s11230-015-9611-y
Moravec F, Bakenhaster M, Buron de I (2013a) A new gonad-infecting species of Philometra (Nematoda: Philometridae) from the Atlantic Spanish mackerel Scomberomorus maculatus (Scombridae) off the Atlantic coast of Florida and South Carolina. J Parasitol. https://doi.org/10.1645/12-39.1
Moravec F, Bakenhaster MD, Seyoum S, Tringali MD (2021) Morphological and genetic description of two new species of philometrid nematodes (Philometridae) parasitic in needlefishes (Belonidae) from estuaries of Florida, USA. Folia Parasitol 68(008)
Moravec F, Barton D (2015) Two gonad-infecting species of Philometra (Nematoda: Philometridae) from marine fishes off the northern coast of Australia. Parasite. https://doi.org/10.1051/parasite/2015008
Moravec F, Barton D (2016) New tissue-dwelling species of Philometra Costa, 1845 and Philometroides Yamaguti, 1935 (Nematoda: Philometridae) from marine perciform fishes off the northern coast of Australia. Syst Parasitol. https://doi.org/10.1007/s11230-016-9657-5
Moravec F, Barton D (2018). New records of philometrids (Nematoda: Philometridae) from marine fishes off Australia, including description of four new species and erection of Digitiphilometroides gen. n. Folia Parasitol. https://doi.org/10.14411/fp.2018.005
Moravec F, Charo-Karisa H, Jirků M (2009). Philometrids (Nematoda: Philometridae) from fishes of Lake Turkana, Kenya, including two new species of Philometra and erection of Afrophilometra gen. n. Folia Parasitol. https://doi.org/10.14411/fp.2009.008
Moravec F, de Buron I (2013). A synthesis of our current knowledge of philometrid nematodes, a group of increasingly important fish parasites. Folia Parasitol. https://doi.org/10.14411/fp.2013.010.
Moravec F, Diggles B (2015a) Philometra mirabilis sp. n. (Nematoda: Philometridae), a new gonad-infecting parasite from the freshwater fish Cichla mirianae (Cichlidae) in Brazilian Amazon. Parasitol Res. https://doi.org/10.1007/s00436-015-4381-7
Moravec F, Diggles B (2015b) A new gonad-infecting species of Philometra, P. barnesi sp. n. (Nematoda: Philometridae), from the marine fish Pomadasys argenteus (Haemulidae) off the northern coast of Australia. Parasitol Res. https://doi.org/10.1007/s00436-015-4641-6
Moravec F, Khosheghbal M, Pazooki J (2013b) Two philometrids (Nematoda: Philometridae) infecting the tigertooth croaker Otolithes ruber (Bloch and Schneider) (Teleostei: Sciaenidae) off Iran, including erection of a new genus. Syst Parasitol. https://doi.org/10.1007/s11230-013-9430-y
Moravec F, Nagasawa K, Nohara K (2012a) Two species of philometrid nematodes (philometridae) from marine fishes off Japan, including Philometroides branchiostegi sp. n. from Branchiostegus japonicus (Malacanthidae). Folia Parasitol. https://doi.org/10.14411/fp.2012.011
Moravec F, Ogawa K (2019) Description of two new species of Philometra Costa, 1845 (Nematoda: Philometridae) from Marine Fishes off Japan, with Notes on Philometroides seriolae (Yamaguti, 1935). Acta Parasitol. https://doi.org/10.2478/s11686-019-00107-y
Moravec F, Shamsi S (2017). Barracudia australiensis n. g. n. sp. (Nematoda: Philometridae) from the obtuse barracuda Sphyraena obtusata Cuvier (Perciformes: Sphyraenidae) off Eastern Australia. Syst Parasitol. https://doi.org/10.1007/s11230-017-9735-3.
Moravec F, Walter T, Yuniar AT (2012b). Five new species of philometrid nematodes (Philometridae) from marine fishes off Java, Indonesia. Folia Parasitol. https://doi.org/10.14411/fp.2012b.017.
Nadler SA, Carreno RA, Mejía-Madrid H, Ullberg J, Pagan C, Houston R, Hugot JP (2007) Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology 134(Pt 10):1421–1442. https://doi.org/10.1017/S0031182007002880
Near TJ, Garey JR, Nadler SA (1998) Phylogenetic relationships of the Acanthocephala inferred from 18S ribosomal DNA sequences Mol Phylogenet Evol https://doi.org/10.1006/mpev.1998.0569
Nei M, Kumar S (2000) Molecular evolution and phylogenetics, 1st edn. Oxford University Press, New York
Negreiros LP, Tavares-Dias M, Elisei C, Tavares LER, Pereira FB (2019) First description of the male of Philometroides acreanensis and phylogenetic assessment of Philometridae (Nematoda: Dracunculoidea) suggest instability of some taxa. Parasitol Int. https://doi.org/10.1016/j.parint.2018.10.010
Oliva ME, Bórquez AS, Olivares AN (1992) Sexual status of Paralabrax humeralis (Serranidae) and infection by Philometra sp. (Nematoda: Dracunculoidea). J Fish Biol. https://doi.org/10.1111/j.1095-8649.1992.tb02645.x
Oliva ME, Castro RE, Burgos R (1996) Parasites of the flatfish Paralichthys adspersus (Steindachner, 1867) (Pleuronectiformes) from northern Chile. Mem Inst Oswaldo Cruz. https://doi.org/10.1590/S0074-02761996000300009
Quiazon KM, Yoshinaga T (2013) Gonad-infecting philometrid Philometra philippinensis sp. nov. (Nematoda, Philometridae) from bigeye barracuda Sphyraena forsteri Cuvier (Sphyraenidae) off Mariveles, Bataan Province, Philippine archipelago. Acta Parasitol. https://doi.org/10.2478/s11686-013-0165-3
Quiazon KMA, Yoshinaga T, Doi H, Araki J, Ogawa K (2014) First description of male Philometra thaiensis Moravec, Fiala et Dyková, 2004 (Nematoda: Philometridae) from the body cavity of the eyespot pufferfish Tetraodon biocellatus Tirant, and evolutionary relationships of this species with other dracunculoids as inferred from SSU rRNA gene sequences. Helminthologia. https://doi.org/10.2478/s11687-014-0235-6
Quiazon KM, Ysohinaga T, Ogawa K (2008) Philometra sawara sp. n. a redescription of Philometra sciaenae Yamaguti, 1941 and Philometra nemipteri Lou, 2001 (Nematoda: Philometridae): a morphological and molecular approach. Folia Parasitol. https://doi.org/10.14411/fp.2008.036
Rambaut A (2009). FigTree v1.3.1. 2006–2009. Program package available at http://tree.bio.ed.ac. Accessed 29 November 2019
Rego AA, Vicente JJ, Santos CP, Wekid RM (1983) Parasitas de anchovas, Pomatomus saltatrix (L.) do Rio de Janeiro. Cienc Cult 35(9):1329–1336
Ronquist F, Teslenkovan M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across large model space. Syst Biol. https://doi.org/10.1093/sysbio/sys029.
Sarmiento L, Tantaleán M, Huiza A (1999) Nemátodos parásitos del hombre y de los animales en el Perú. Rev Peruana Parasitol 14:9–65
Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464
Seo H-G, Seo JS, Ryu MK, Lee EH, Jung SH, Han H-J (2015) Molecular identification and development of a PCR assay for the detection of a philometrid nematode in Rockfish Sebastes schlegeli. Korean J Fish Aq Sci. https://doi.org/10.5657/KFAS.2015.0731
Sokolov, S. G., Kalmykov, A. P., and Malysheva, S. V. (2020). Phylogeny of dracunculoid nematodes (Chromadorea: Rhabditida: Spirurina: Dracunculoidea) from some Eurasian freshwater fishes. Zootaxa. https://doi.org/10.11646/zootaxa.4858.4.3
Svitin, R., Schoeman, A. L., and Du Preez, L. H. (2018). New information on morphology and molecular data of camallanid nematodes parasitising Xenopus laevis (Anura: Pipidae) in South Africa. Folia Parasitol. https://doi.org/10.14411/fp.2018.003.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. https://doi.org/10.1093/molbev/mst197.
Tkach V, Littlewood T, Olson P, Kinsella JM, Swiderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea) Syst Parasitol https://doi.org/10.1023/A:1025546001611
Travassos L, Artigas P, Pereira C (1928) Fauna helminthological dos peixes do agua doce do Brasil. Arq Inst Biol (s Paulo) 1:5–68
Vaz Z, Pereira C (1934) Contribuição ao conhecimento dos nematoides de peixes fluviais do Brasil. Arq Inst Biol (s Paulo) 5:87–103
Wang S-X, Li L, Zhang L-P (2015) Redescription and genetic characterization of Philometra lagocephali Moravec et Justine 2008 (Nematoda: Philometridae) from Lagocephalus lunaris (Bloch and Schneider) (Tetraodontiformes: Tetradontidae) in the South China Sea. Acta Parasitol. https://doi.org/10.1515/ap-2015-0055
Wijová M, Moravec F, Horák A, Lukeš J (2006) Evolutionary relationships of Spirurina (Nematoda: Chromadorea: Rhabditida) with special emphasis on dracunculoid nematodes inferred from SSU rRNA gene sequences. Int J Parasitol. https://doi.org/10.1016/j.ijpara.2006.04.005
WoRMS (2022). Philometroides Yamaguti, (1935). http://www.marinespecies.org/aphia.php?p=taxdetailsandid=390961 Accessed 08 July 2021.
Wu S-G, Wang G-T, Li W-X, Nie P (2005) A preliminary study on phylogeny of nine species of philometrids in China. Acta Hydrobiol Sin 29(5):571–575
Acknowledgements
We are grateful to the authorities of OPDS (Organismo Provincial para el Desarrollo Sostenible) and Administration Parques Nacionales for granting us the permits to carry out fieldwork in Refugio de vida Silvestre Bahía Samborombón and Campos del Tuyú National Park, to the park rangers and staff of Parques Nacionales for field assistance, and to CEPAVE for providing the resources needed to undertake this work.
Funding
This research was supported by Agencia Nacional de Promoción Científica y Técnica (PICT 34412/05 and PICT 2358/2015) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 0015, and PIP 11220150100705CO).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional guides on the care and use of animals.
Consent to participate
All the authors give their consent to participate in this work.
Consent for publication
All the authors give their consent to the publication of this work.
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Matthew Thomas Wayland
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Montes, M.M., Acosta Albarracin, M., Barneche, J. et al. Molecular phylogenetic relationship between Philometroides tahieli (Nematoda, Philometridae) and other philometrids from South America. Parasitol Res 121, 3091–3103 (2022). https://doi.org/10.1007/s00436-022-07652-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-022-07652-y