Skip to main content
SpringerLink
Log in

Phylogenetic position of Diplostomum spp. from New World herons based on complete mitogenomes, rDNA operons, and DNA barcodes, including a new species with partially elucidated life cycle

  • Fish Parasitology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Diplostomum ardeae Dubois, 1969 has seldom been reported since its description from the great blue heron (Ardea herodias L., 1758) in the USA. Sequences obtained in this study from the barcode region of cytochrome c oxidase 1 (CO1) in diplostomids from black-crowned night heron (Nycticorax nycticorax (L., 1758)) in Puerto Rico matched data from D. ardeae from A. herodias in the type region. We also obtained DNA barcodes from morphologically similar diplostomids from a rufescent tiger heron (Tigrisoma lineatum (Boddaert, 1783)) and from metacercariae from eye lenses of Trachelyopterus galeatus (Linnaeus, 1766) from the Paraná River basin in Argentina and Brazil, respectively. Barcodes matched (97–100% identity) in these South American adult and larval specimens as well as in recently published sequences from metacercariae from 11 other siluriform fishes from the same region. Barcodes from the South American species, which we describe as Diplostomum lunaschiae n. sp., differed from those of D. ardeae by 7.2–9.8%, and the new species differs from D. ardeae in its size, pharynx:oral sucker length ratio, egg:body length ratio, and distribution of vitellaria. As in prior phylogenetic analysis of CO1 sequences, both D. ardeae and D. lunaschiae n. sp. were not associated with Diplostomum. In more character-rich analyses of nuclear rDNA and of mitochondrial genomes, D. ardeae was an early divergent member of clades of species of Diplostomum. Consequently, we continue to consider D. ardeae and D. lunaschiae n. sp. members of Diplostomum, in contrast to recent suggestions that these species may belong to a different genus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Nucleotide sequences reported here are available in GenBank (D. ardeae mitochondrial genome MT259035 and rDNA operon MT259036; D. ardeae and D. lunaschiae n. sp. CO1 DNA barcodes MT324592-626), and vouchers have been deposited at the Museum of Southwestern Biology (MSB: Para:30692-3) and Museo de La Plata (MLP-He 7656).

References

  • Acosta AA, Smit NJ, da Silva RJ (2020) Diversity of helminth parasites of eight siluriform fishes from the Aguapeí River, Upper Paraná basin, São Paulo State, Brazil. Int J Parasitol Parasites Wildl 11:120–128. https://doi.org/10.1016/j.ijppaw.2020.01.003

    Article  PubMed  PubMed Central  Google Scholar 

  • Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69:313–319. https://doi.org/10.1016/j.ympev.2012.08.023

    Article  PubMed  Google Scholar 

  • Bunkley-Williams L, Williams EH (1994) Parasites of Puerto Rican freshwater sport fishes. Puerto Rico Department of Natural and Environmental Resources, San Juan, PR and Department of Marine Sciences, University of Puerto Rico, Mayaguez, PR, 168 pp

  • Dronen NO, Chen W-C (2002) Endohelminths from the little blue heron Egretta caerulea from the Texas Gulf Coast. Comp Parasitol 69:96–99. https://doi.org/10.1654/1525-2647(2002)069[0096:EFTLBH]2.0.CO;2

    Article  Google Scholar 

  • Dubois G (1969) Les Strigeata (Trematoda) de la collection Elizabeth M. Boyd. Bull. Société Neuchâtel Sci Nat 92:5–12. https://doi.org/10.5169/seals-88991

  • Dubois G (1970) Synopsis des Strigeidae et des Diplostomatidae (Trematoda). Mém Société Neuchâtel Sci Nat 10:1–727

  • Dubois G, Angel M (1972) Strigeata of Australian birds and mammals from the helminthological collection of the University of Adelaide. Trans R Soc S Aust 96:197–215

    Google Scholar 

  • El-Naffar M, Khalifa R, Sakla A (1980) Parasitofauna of the Egyptian aquatic birds. II. Trematode parasites of the giant heron (Ardea goliath) in Assiut governorate. J Egypt Soc Parasitol 10:107–116

    Google Scholar 

  • Gómez JP, López HL (2015) Dibujantes del Museo de La Plata: Luis Gerardo Pagano. ProBiota, Serie Arte y Sociedad en la Ictiología Nacional, 10:1–30

  • Graça WJ, Pavanelli CS (2007) Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. EDUEM, Maringá

  • Hernández-Mena DI, García-Varela M, de León GP (2017) Filling the gaps in the classification of the Digenea Carus, 1863: systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences. Syst Parasitol 94:833–848. https://doi.org/10.1007/s11230-017-9745-1

    Article  PubMed  Google Scholar 

  • Hoffman GL, Hundley JB (1957) The life-cycle of Diplostomum baeri eucaliae n. subsp. (Trematoda: Strigeida). J Parasitol 43:613–627

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leite LAR, Pelegrini LS, Agostinho BN, Azevedo RK, Abdallah VD (2018) Biodiversity of the metazoan parasites of Prochilodus lineatus (Valenciennes, 1837) (Characiformes: Prochilodontidae) in anthropized environments from the Batalha River, São Paulo State, Brazil. Biot Neotrop 18:e20170422. https://doi.org/10.1590/1676-0611-BN-2017-0422

    Article  Google Scholar 

  • Locke SA, Al-Nasiri FS, Caffara M, Drago F, Kalbe M, Lapierre AR, McLaughlin JD, Nie P, Overstreet RM, Souza GT, Takemoto RM, Marcogliese DJ (2015) Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. Int J Parasitol 45:841–855. https://doi.org/10.1016/j.ijpara.2015.07.001

    Article  PubMed  CAS  Google Scholar 

  • Moszczynska A, Locke SA, McLaughlin JD, Marcogliese DJ, Crease TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Mol Ecol Resour 9:75–82. https://doi.org/10.1111/j.1755-0998.2009.02634.x

    Article  PubMed  CAS  Google Scholar 

  • Neal JW, Lilyestrom CG, Kwak TJ (2009) Factors influencing tropical island freshwater fishes: species, status, and management implications in Puerto Rico. Fisheries. 34:546–554. https://doi.org/10.1577/1548-8446-34.11.546

    Article  Google Scholar 

  • Pelegrini LS, Gião T, Vieira DH, Müller MI, da Silva RJ, Pérez-Ponce de León G, de Azevedo RK, Abdallah VD (2019) Molecular and morphological characterization of the metacercariae of two species of diplostomid trematodes (Platyhelminthes, Digenea) in freshwater fishes of the Batalha River, Brazil. Parasitol Res 118:2169–2182. https://doi.org/10.1007/s00436-019-06362-2

    Article  PubMed  Google Scholar 

  • Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337. https://doi.org/10.1007/s13127-011-0056-0

    Article  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van der Schalie H (1948). The land and fresh-water mollusks of Puerto Rico. University of Michigan Press, Ann Arbor, 134 pp

  • Xia X, Lemey P (2009) Assessing substitution saturation with DAMBE. In: Lemey P, Salemi M, Vandamme A-M (eds) The phylogenetic handbook: a practical approach to phylogenetic analysis and hypothesis testing. Cambridge University Press, Cambridge, pp 615–630

    Chapter  Google Scholar 

  • Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7. https://doi.org/10.1016/S1055-7903(02)00326-3

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Three anonymous reviewers provided comments on earlier drafts that improved this article. Susan Wylie and staff at Le Nichoir, Hudson, Quebec, provided access to a salvaged carcass of A. herodias. Fieldwork in Formosa was conducted with Agustín M. Abba (CONICET) and our departed colleague and friend, Luis Gerardo Pagano (1985–2020), some of whose contributions are reviewed by Gómez and López (2015).

Funding

This study was financially supported by the Puerto Rico Science, Technology and Research Trust (grant 2016-00080); the National Science Foundation’s Division of Environmental Biology (grant 1845021); Paul D. N. Hebert (University of Guelph) through funding from NSERC, Genome Canada, the Ontario Genomics Institute and the International Barcode of Life; Universidad Nacional de La Plata (11/N896); the Comisión de Investigaciones Científicas de la provincia de Buenos Aires (Res. 597/16), Argentina; CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (process 13741-12-8); and the CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico (process 480180/2011-3).

Author information

Authors and Affiliations

  1. Departamento de Biología, University of Puerto Rico at Mayagüez, Box 9000, Mayagüez, 00681–9000, Puerto Rico

    Sean A. Locke

  2. División Zoología Invertebrados, Museo de La Plata, Paseo del Bosque S/N, 1900, La Plata, Buenos Aires, Argentina

    Fabiana B. Drago & Verónica Núñez

  3. Instituto Federal de São Paulo, IFSP - campus Avaré. Avenida Professor Celso Ferreira da Silva Jardim Europa I, Avaré, SP, 18707150, Brazil

    Geza Thais Rangel e Souza

  4. Center of Biological Sciences, Nupelia – Icthyoparasitology Laboratory, State University of Maringá, Av Colombo, No. 5790, Block G90, room 11, villa 7, Maringá, PR, 87020-900, Brazil

    Geza Thais Rangel e Souza & Ricardo M. Takemoto

Authors
  1. Sean A. Locke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabiana B. Drago
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Verónica Núñez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Geza Thais Rangel e Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ricardo M. Takemoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sean A. Locke.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Section Editor: Guillermo Salgado-Maldonado

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Locke, S.A., Drago, F.B., Núñez, V. et al. Phylogenetic position of Diplostomum spp. from New World herons based on complete mitogenomes, rDNA operons, and DNA barcodes, including a new species with partially elucidated life cycle. Parasitol Res 119, 2129–2137 (2020). https://doi.org/10.1007/s00436-020-06713-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-06713-4

Keywords

Search

Navigation