Abstract
The family Bucephalidae is comprised of nine subfamilies, the most important being Bucephalinae with eight genera. Among these, the genus Rhipidocotyle has been found in marine and freshwater environments all over the world. Previous studies of Rhipidocotyle santanaensis have dealt with its morphology or host’s ecology. Here, we provide a phylogenetic analysis based on two 28S rDNA sequences from R. santanaensis parasitizing the freshwater fish Acestrorhynchus pantaneiro from the Ibera Lagoon (Corrientes Province, Argentina). The 28S rDNA tree showed that it clustered together with Rhipidocotyle species from Middle and North America, suggesting a common history. Bucephalinae appears to have undergone four evolutionary processes: first, the diversification within the same host family; second, more than one successful infection of the same host family in different geographic regions; third, “jumping” between host families; and, finally, successful invasion of the freshwater environment (occurring in at least four different events in the subfamily). We hypothesize that R. santanaensis entered the freshwater environment by a “jumping” event from some unknown marine host family when a seawater ingression took place in South America during the Late Quaternary. This is the first sequenced Bucephalinae species from South America. Further sequencing will help shed light on the evolutionary relationships between South American members of this group from marine and, especially, freshwater environments.
Similar content being viewed by others
Data availability
Slides are deposited in the MLP under accessions MLP- He 7981. DNA sequences are deposited in GenBank under accessions OQ244080-81.
References
Atopkin D, Shedko M, Rozhkovan K, Nguyen H, Besprozvannykh V (2022) Rhipidocotyle husi n. sp. and three known species of Bucephalidae Poche, 1907 from the East Asian Region: morphological and molecular data. Parasitology 149:774–785. https://doi.org/10.1017/S0031182022000208
Baba T, Nakamura D, Hosoi M, Urabe M (2012) Molecular identification of larval Bucephalids, Prosorhynchoides ozakii and Parabucephalopsis parasiluri, infecting the golden mussel Limnoperna fortunei, by PCR-RFLP. J Parasitol 98:669–673. https://doi.org/10.1645/GE-2837.1
Bray RA, Webster BL, Bartoli P, Littlewood DTJ (2005) A molecular phylogenetic study of the Acanthocolpidae (Digenea). Acta Parasitol 50:281–291
Corner RD, Cribb TH, Cutmore SC (2020) A new genus of Bucephalidae Poche, 1907 (Trematoda: Digenea) for three new species infecting the yellowtail pike, Sphyraena obtusata Cuvier (Sphyraenidae), from Moreton Bay, Queensland, Australia. Syst Parasitol 97:455–476. https://doi.org/10.1007/s11230-020-09931-7
Fernandes BMM, Justo MCN, Anjos CSD, Malta JCO, Dumbo JC (2017) Digenea parasites of Acestrorhynchus falcirostris (Osteichthyes, Acestrorhynchidae) in the state of Amazonas, Brazil. Rev Bras Parasitol Vet 26:439–445. https://doi.org/10.1590/S1984-29612017059
Hammond MD, Cribb TH, Bott NJ (2018) Three new species of Prosorhynchoides (Digenea: Bucephalidae) from Tylosurus gavialoides (Belonidae) in Moreton Bay, Queensland, Australia. Parasitol Int 67:454–464. https://doi.org/10.1016/j.parint.2018.04.004
Hammond MD, Cribb TH, Nolan MJ, Bott NJ (2020) Two new species of Prosorhynchoides (Digenea: Bucephalidae) from Tylosurus crocodilus (Belonidae) from the Great Barrier Reef and French Polynesia. Parasitol Int 75:102005. https://doi.org/10.1016/j.parint.2019.102005
Katoh K, Rozewicki J, Yamada K (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. https://doi.org/10.1093/bib/bbx108
Kohn A, Fernandes BM, Cohen SC (2007) South American trematodes parasites of fishes. Express Ltda, Sao Paulo
Kumar S, Stecher G, LiM KC, Tamura K (2018) Mega X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Littlewood DTJ, Curini-Galletti M, Herniou EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol Phylogenet Evol 16:449–466. https://doi.org/10.1006/mpev.2000.0802
Lunaschi LI (2004) Two new species of bucephalids (Digenea: Bucephalidae) parasitic in freshwater fishes of Argentina. Parasitol Int 53:229–234. https://doi.org/10.1016/j.parint.2004.01.014
Mirande J, Koerber J (2020) Checklist of the freshwater fishes of Argentina. Ichthiol Contr Peces Criollos 72:1–81
Nolan MJ, Curran SS, Miller TL, Cutmore SC, Cantacessi C, Cribb TH (2015) Dollfustrema durum n. sp. and Heterobucephalopsis perardua n. sp. (Digenea: Bucephalidae) from the giant moray eel, Gymnothorax javanicus (Bleeker) (Anguilliformes: Muraenidae), and proposal of the Heterobucephalopsinae n. subfam. Parasitol Int 64:59–570. https://doi.org/10.1016/j.parint.2015.07.003
Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755. https://doi.org/10.1016/S0020-7519(03)00049
Overstreet RM, Curran SS (2002) Superfamily Bucephaloidea Poche, 1907. In: Keys to the Trematoda: Volume 1. CABI Publishing, Wallingford UK, pp 67–110
Pedro NHO, Pelegrini LS, Azevedo RK, Abdallah VD (2016) First record of Rhipidocotyle santanaensis (Digenea) parasitizing Acestrorhynchus lacustris from Batalha River, Brazil. Braz J Biol 76:878–883. https://doi.org/10.1590/1519-6984.02515
Pereyra FX, Baumann V, Altinier V, Ferrer J, Tchilinguirian P (2004) Soil genesis and landscape evolution in the Parana River Delta. Rev Asoc Geol Arg 59:229–242. http://hdl.handle.net/20.500.12110/paper_00044822_v59_n2_p229_Pereyra. Accessed 9 Jul 2022
Pérez-Ponce de León G, Hernandez Mena DI (2019) Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ Tree of Life. J Helminthol 93:260–276. https://doi.org/10.1017/S0022149X19000191
Petkevičiūtė R, Stunžėnas V, Staneviciute G (2014) Differentiation of European freshwater bucephalids (Digenea:Bucephalidae) based on karyotypes and DNA sequences. Syst Parasitol 87:199–212. https://doi.org/10.1007/s11230-013-9465-0
Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808
Pritchard MH, Kruse GOW (1982) The collection and preservation of animal parasites. University of Nebraska Press, Nebraska, p 141
Ronquist F, Teslenkovan M, van der Mark P, Ayres DL, Darling A, Hohna 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 61:539–542. https://doi.org/10.1093/sysbio/sys029
Shirakashi S, Waki T, Ogawa K (2020) Bucephalid metacercarial infection in wild larval and juvenile Ayu Plecoglossus altivelis. Fish Pathol 54:93–100. https://doi.org/10.3147/jsfp.54.93
Stunžėnas V, Cryan JR, Molloy DP (2004) Comparison of rDNA sequences from colchicine treated and untreated sporocysts of Phyllodistomum folium and Bucephalus polymorphus (Digenea). Parasitol Int 53:223–228. https://doi.org/10.1016/j.parint.2003.12.003
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. https://doi.org/10.1080/10635150701472164
Tkach V, Littlewood D, Olson P, Kinsella J, Swiderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst Parasitol 56:1–15. https://doi.org/10.1023/A:1025546001611
Úbeda B, Di Giacomo AS, Neiff JJ, Loiselle SA, Guadalupe Poi AS, Gálvez JA, Casco S, Cózar A (2013) Potential Effects of Climate Change on the Water Level, Flora and Macro-fauna of a Large Neotropical Wetland. PLoS ONE 8:e67787. https://doi.org/10.1371/journal.pone.0067787
WoRMS (2022) Bucephalinae Poche, 1907. https://www.marinespecies.org/ aphia.php?p=taxdetails&id =579575 accessed 7 July 2022
Acknowledgements
We are grateful to the authorities of Municipio Colonia Carlos Pellegrini, Corrientes Province, Argentina, for granting us the permits to carry out fieldwork, to the park rangers of the Iberá Provincial Reserve, to the people of Colonia C. Pellegrini for their kind assistance, and to CEPAVE for providing the facilities for this work. Finally, special thanks are due to Silvia Pietrokovsky and PhD Tyler J. Achatz for the revising our use of the English language in the manuscript.
Funding
This research was partially supported by the Agencia Nacional de Promoción Científica y Técnica (PICT 2020 SERIE A-01531), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET, PIP 1713), and Universidad Nacional de La Plata (PPID N902 and N039).
Author information
Authors and Affiliations
Contributions
Martin M. Montes: Specimen collection, morphological and molecular study of parasites, phylogenetic analysis, principal writer of the manuscript.
Clara Vercellini: Secondary writer of the manuscript, text formatting.
Nicolas Ostoich: Morphological study of parasites.
Marina Ibañez Shimabukuro: Molecular study of parasites.
Gastón Cavallo: Parasite imaging and figure preparation.
German Reig Cardarella: Manuscript editing.
Sergio Martorelli: Obtaining funding, manuscript preparation supervision.
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: Shokoofeh Shamsi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
Supplementary material 1 Photos of Rhipidocotyle santanaensis Lunaschi, 2014 from Ibera Lagoon, Corrientes Province, Argentina. (TIF 54101 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) 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., Vercellini, C., Ostoich, N. et al. Phylogenetic position of the South American freshwater Rhipidocotyle santaensis (Digenea:Bucephalidae) based on partial 28S rDNA. Parasitol Res 122, 1765–1774 (2023). https://doi.org/10.1007/s00436-023-07863-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-023-07863-x