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Phylogenetic Position of Diplostomum Spp. from New World Herons Based

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Phylogenetic Position of Diplostomum Spp. from New World Herons Based Parasitology Research https://doi.org/10.1007/s00436-020-06713-4 FISH PARASITOLOGY - ORIGINAL PAPER 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 Sean A. Locke1 & Fabiana B. Drago2 & Verónica Núñez2 & Geza Thais Rangel e Souza3,4 & Ricardo M. Takemoto4 Received: 14 February 2020 /Accepted: 10 May 2020 # Springer-Verlag GmbH Germany, part of Springer Nature 2020 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.Inmorecharacter-richanalysesof 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,incontrasttorecent suggestions that these species may belong to a different genus. Keywords Eye fluke . Catfish . Neotropic . Diplostomoidea . Phylogeny . Genomics Introduction Dubois (1969) described Diplostomum ardeae from three specimens from a great blue heron (Ardea herodias L., Section Editor: Guillermo Salgado-Maldonado 1758, Ardeidae, Pelecaniformes) collected in Hampden County, Massachusetts. El-Naffar et al. (1980) used the pre- * Sean A. Locke [email protected] occupied name of D. ardeae to describe a species from Ardea goliath Cretzschmar, 1829 in Egypt, but this species bears little resemblance to D. ardeae Dubois, 1969, differing mark- 1 Departamento de Biología, University of Puerto Rico at Mayagüez, Box 9000, Mayagüez 00681–9000, Puerto Rico edly in the morphology of eggs, prepharynx, pseudosuckers, and relative lengths of the fore- and hindbody. Diplostomum 2 División Zoología Invertebrados, Museo de La Plata, Paseo del Bosque S/N, 1900 La Plata, Buenos Aires, Argentina ardeae was next reported from 3 of 13 Egretta caerulea (L., 1758) (Ardeidae) examined by Dronen and Chen 2002 in 3 Instituto Federal de São Paulo, IFSP - campus Avaré. Avenida Professor Celso Ferreira da Silva Jardim Europa I, coastal Texas, about 2500 km southeast of the type locality. Avaré, SP 18707150, Brazil Locke et al. (2015) published a partial sequence of cyto- 4 Center of Biological Sciences, Nupelia – Icthyoparasitology chrome c oxidase I (CO1) from D. ardeae from A. herodias Laboratory, State University of Maringá, Av Colombo, No. 5790, collected approximately 400 km northwest of the type locali- Block G90, room 11, villa 7, Maringá, PR 87020-900, Brazil ty. Pelegrini et al. (2019) sequenced the same (barcode) region Parasitol Res of CO1 in metacercariae resembling the adult form of June, 2011 (Table 1). Fish were identified according to D. ardeae from the eye lenses of 11 species in three families Graça and Pavanelli (2007) and sacrificed by spinal section of siluriform fishes in Brazil. The CO1 sequences of these with the authorization of the Ethics Council of the State larval parasites diverged by 6.9–7.6% from D. ardeae,leading University of Maringá (CEAE - Opinion 123/2010). In spec- Pelegrini et al. (2019) to conclude they belong to a species imens of Trachelyopterus galeatus (Linnaeus, 1766), one eye closely related to D. ardeae.PhylogeneticanalysesofCO1 was fixed in 10% formalin, embedded in paraffin, and sec- sequences suggest both the Brazilian species and D. ardeae tioned with a microtome into 5-μm slices that were stained are not allied with Diplostomum or other diplostomid genera with hematoxylin and eosin and photographed on slides with from which data are available (Locke et al. 2015;Hernández- phase contrast using a Nikon Eclipse E200 microscope Mena et al. 2017; Pelegrini et al. 2019). Pelegrini et al. (2019) coupled to a Samsung DV100 camera. Parasites in the other also noted that the metacercariae they examined presented eye of the same individual T. galeatus were preserved in 70% morphological inconsistencies with species of Diplostomum, ethanol and refrigerated in 95% ethanol until DNA extraction. particularly the relative lengths of the fore- and hindbody and the distribution of vitellaria. We also note that most species of DNA extraction, PCR amplification, and sequencing Diplostomum mature in members of the Charadriformes, rath- er than pelecaniform hosts such as ardeids (Dubois 1970; DNA extracted from individual worms (or worm subsamples) Dubois and Angel 1972). was analyzed with the aim of determining whether the sam- In this study, we conducted additional molecular analysis ples collected in different localities and hosts represented the to further evaluate the generic affiliation of D. ardeae and we same species, and whether they could be placed in a known report additional sequence-based records that enlarge the genus. Barcode sequences of CO1 were obtained using the geographic and host range of this species. We describe the extraction methods, diplostomid-specific primers, and proto- adult form of the species Pelegrini et al. (2019)encountered cols of Moszczynska et al. (2009). DNA from a specimen of as metacercariae and report additional records of its larval D. ardeae from N. nycticorax from Puerto Rico was shotgun forms. sequenced in a tenth of a lane on an Illumina HiSeq 4000, and 150-bp paired-end libraries were built with Nextera adapters at Genewiz (NJ). To assemble Illumina reads into a mitochon- Materials and methods drial genome, data from D. spathaceum (Rudolphi, 1819) (KR269763) were used as a scaffold in Geneious Prime Specimen collection and identification 2019 (www.geneious.com) using default parameters. The longest resulting fragment assembled with good coverage Immature adult diplostomids were collected from the small (3407 bp, ≥ 183 reads per site) was then used to seed intestine of a road-killed black-crowned night heron iterative assemblies from the total read pool, extending to (Nycticorax nycticorax (L., 1758)) found near Yauco, Puerto the whole mitochondrion, and the final assembly was Rico (18.0131, − 66.8963) in June, 2017. Mature adult annotated using MITOS (Bernt et al. 2013) and by alignment diplostomids were collected from the small intestine of a ru- with D. spathaceum (KR269763) and D. pseudospathaceum fescent tiger heron (Tigrisoma lineatum (Boddaert, 1783)) Niewiadomska, 1984 (KR269764). The rDNA operon was shot in 2016 at Marcela Farm, Formosa Province, Argentina assembled iteratively using as an initial scaffold a consensus (− 26.2930, − 59.1439) with authorization of the Ministerio de from an alignment of sequences from Diplostomum spp. la Producción, Dirección de Fauna y Parques of Formosa. (KR269765-6) and Tylodelphys immer Dubois, 1961 Specimens were preserved in 95% ethanol, later rehydrated, (MH521252) with default parameters in Geneious. stained in dilute acetocarmine, dehydrated in ethanol, cleared Sequences were aligned with representative, published data in clove oil or xylol, and mounted on a slide in Canada from diplostomids, including data from Pelegrini et al. (2019). balsam, and studied and drawn with the aid of an ocular Because of substantial saturation (ISS = 0.573, ISS.cAsym = micrometer and camera lucida. Two paragenophores of a 0.516, T = 1.198, DF = 115, P =0.23;Xiaetal.2003, Xia and specimen of D. ardeae from A. herodias in Montreal, Lemey 2009), the third codon was removed from the phylo- Quebec, in which CO1 was sequenced by Locke et al. genetic analysis of CO1. In the CO1 phylogeny and others (2015) (KR271033), were also studied morphologically and (see below), alignments were stripped of gaps and redundant are newly deposited in the Museum of Southwestern Biology sequences, and models of nucleotide evolution were selected (MSB:Para: 30692). Metacercariae were collected from the using Bayesian Information Criterion in MEGA-X (Kumar eyes of 837 fish in 56 species caught with nets at several et al. 2018). Genetic distances (uncorrected p) are reported localities (Ivinhema, Baía, and Paraná Rivers) in the upper based on all sites and sequences. Phylogenetic trees were con- Paraná River floodplain along the borders of states Paraná structed with 1000 bootstrap replicates with RAXML and Mato Grosso do Sul (− 22.8230, − 53.4378), Brazil, in (Silvestro and Michalak 2012; Stamatakis 2014) and using Parasitol Res Table 1 Fish examined in Paraná River floodplain (Paraná and Mato Table 1 (continued) Grosso do Sul, Brazil)
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