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(Nematoda: Rhabdiasidae) from the Lancehead Snake Bothrops Moojeni Hoge, 1966 (Reptilia: Serpentes: Viperidae) in Brazil

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(Nematoda: Rhabdiasidae) from the Lancehead Snake Bothrops Moojeni Hoge, 1966 (Reptilia: Serpentes: Viperidae) in Brazil Journal of Helminthology (2017) 91, 360–370 doi:10.1017/S0022149X16000377 © Cambridge University Press 2016 Morphometric and phylogenetic analyses of Serpentirhabdias viperidicus n. sp. (Nematoda: Rhabdiasidae) from the lancehead snake Bothrops moojeni Hoge, 1966 (Reptilia: Serpentes: Viperidae) in Brazil D.H. Morais*, A. Aguiar, M.I. Müller, R.B. Narciso, L.A.F. da Silva and R.J. da Silva UNESP – Univ. Estadual Paulista, Campus de Botucatu, Instituto de Biociências, Departamento de Parasitologia, Av. Bento Lopes s/n Distrito de Rubião Junior CEP 18080-970, Botucatu, SP, Brazil (Received 11 February 2016; Accepted 19 May 2016; First published online 27 June 2016) Abstract Serpentirhabdias viperidicus n. sp. (Nematoda: Rhabdiasidae) is described from the lungs of the ‘Brazilian lancehead’ Bothrops moojeni (Hoge, 1966) from the sa- vannah in São Paulo State, Brazil. The new species is the eighth species of Serpentirhabdias described in the Neotropical region, and differs from other spe- cies mainly by a combination of characters: lips slightly notable, presence of fine striations at posterior ends, presence of two parallel lines with intercalated pores, a pore-shaped phasmid situated at the level of the anal aperture and another two in the posterior half of the tail. It is the first species of Serpentirhabdias reported in this snake host and the second species of this genus found parasitizing South American viperidian snakes. Molecular phylogenetic analysis using ribosomal (ITS and 28S partial) genes confirms Serpentirhabdias viperidicus n. sp. as a new species that clustered in the Serpentirhabdias clade, sister taxon to Serpentirhabdias fuscovenosa and Serpentirhabdias elaphe. This is the first description of Serpentirhabdias species from Brazil using molecular approaches and morpho- logical characters to confirm the monophyly of this recent genus. Introduction 1905, Kurilonema Szczerbak & Shapilo, 1969, Neoentomelas Hasegawa, 1989, Pneumonema Johnston, 1916, and Ento- Nematodes of the family Rhabdiasidae are commonly melas Travassos, 1930. Given their particular morphologic- found in association with the lungs of amphibians and al and biological characters (comparatively thin body reptiles worldwide. They are found in Australian, cuticle, arrangement of lips in two lateral groups, smaller Ethiopian, Palaearctic, Oriental and Neotropical regions number of eggs, presence of homogony in the life cycles (Kuzmin, 2013; Tkach et al., 2014, Kuzmin & Tkach, and restricted specificity to snakes) and molecular studies, 2015). Recently, the genus Serpentirhabdias was proposed 14 species of Rhabdias were transferred to Serpentirhabdias by Tkach et al.(2014) in addition to the genera (Tkach et al., 2014). Acanthorhabdias Pereira, 1927, Rhabdias Stiles & Hassall, Seven species of Serpentirhabdias are known from the Neotropical region, of which six are parasites of colubroi- dean snakes, as follows: S. cf. fuscovenosa (Railliet, 1899), *E-mail: [email protected] S. labiata (Pereira, 1927), S. vellardi (Pereira, 1928), S. lamothei Downloaded from https://www.cambridge.org/core. UNESP, on 22 Jul 2019 at 14:32:58, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0022149X16000377 Description of Serpentirhabdias viperidicus n. sp. 361 (Martínez-Salazar & León-Régagnon, 2006), S. filicaudalis morphometry of some Serpentirhabdias spp. from the (Barrella, Santos & Silva, 2009) and S. atracti Kuzmin, Neotropical region are given in table 1. Melo & Santos, 2014 (Barella et al., 2010; Kuzmin et al., 2014); and only S. atroxi Kuzmin, Giese, Melo, Costa, Molecular analysis Maschio & Santos, 2016 has been reported in viperidian snakes. Among these nematodes, five have been recorded For molecular analysis, some specimens were fixed in in snakes from Brazil, S. vellardi in Philodrias patagoniensis absolute ethanol (Merck®) and cut in pieces. Part was (=Philodrias schotti) (Colubridae) and Oxyrhopus trigeminus taken for scanning electron microscopy and part for (Dipsadidae), S. labiata in Xenodon merremi (=Rhadinea DNA extraction. Genomic DNA was extracted from merremi) (Dipsadidae), S. filicaudalis in Spilotes pullatus parts of single specimens of worms using DNeasy® (Colubridae), S. atracti in Atractus major (Dipsadidae) Blood and Tissue Kit (Qiagen, California, USA) according and S. atroxi in Bothrops atrox (Viperidae) (Pereira, 1927, to the manufacturer’s protocol, with a final volume of 1928; Barella et al., 2010; Kuzmin et al., 2014, 2016). 50 μl. DNA fragments were amplified using 28S (partial) Pit vipers of the genus Bothrops are among the best- containing D2/D3 divergent domains, internal tran- studied most wide-ranging Neotropical snake clades scribed spacer (ITS; complete) and cytochrome c oxidase (Carrasco et al., 2012). Even with this extensive accumu- I (COI) genes. Primers and cycling conditions are pre- lated knowledge on natural history, taxonomy and phylo- sented in table 2. genetic relationships (Fenker et al., 2014), only S. atroxi of Amplification reactions consisted of 25 μl primary poly- the Rhabdiasidae was reported parasitizing a snake spe- merase chain reaction (PCR) amplifications, with 3 μl cies of the Bothrops genus (B. atrox) (Kuzmin et al., 2016). DNA extract, 0.5 or 1.0 μl of each primer and In addition, there is no study on the nematode fauna of Ready-to-Go PCR beads (Pure Taq™ Ready-to-Go™ Bothrops moojeni, a large pit viper from riparian areas in PCR beads, GE Healthcare, Chicago, USA). The solution central and south-eastern Brazil, throughout the Cerrado consisted of stabilizers, bovine serum albumin (BSA), morphoclimatic domain (Leloup, 1984; Campbell & deoxyadenosine triphosphate (dATP), deoxycytidine tri- Lamar, 1989; Borges & Araújo, 1998; Nogueira et al., phosphate (dCTP), deoxyguanosine triphosphate 2003; Fenker et al., 2014). (dGTP), deoxythymidine triphosphate (dTTP), 2.5 units During a survey of parasites from B. moojeni snakes in of puReTaq DNA polymerase and reaction buffer. With São Paulo State, Brazil, nematodes of the genus the reconstituted bead at a final volume of 25 μl, the con- Serpentirhabdias were located in the lungs and identified centration of each deoxynucleoside triphosphate (dNTP) as Serpentirhabdias viperidicus n. sp. using morphological was 200 μM in 10 mM Tris–HCl (pH 9.0 at room tempera- and molecular phylogenetic analyses. ture), 50 mM KCl and 1.5 mM MgCl2. PCR products (2 μl) were run on agarose gel (1%) using gel red and loading buffer to confirm amplicon size and Materials and methods yield. PCR products were purified using QIAquick PCR Purification Kit (Qiagen) and automated sequencing was Collection and examination of nematodes performed directly on purified PCR products from speci- During a helminthological survey in the period be- mens using BigDye v.3.1 Terminator Cycle Sequencing tween July 2012 and February 2013, 12 specimens of B. Ready Reaction kit (Applied Biosystems, Foster City, moojeni were collected at ‘Reserva Particular do California, USA) for cycle sequencing. Sequences were Patrimônio Natural Foz do Rio Aguapeí’, municipality run on an Applied Biosystems ABI 3500 DNA genetic ana- of Castilho, São Paulo State, Brazil (license permission lyser. The sequence identity was verified using the Basic SISBIO 30772-4). The snakes were euthanized by injection Local Alignment Search Tool (BLAST) and contiguous se- of sodium thiopental and necropsied for parasite survey quences were assembled and edited using Sequencher under a stereomicroscope. A total of 115 nematodes v. 5.2.4 (Gene Codes, Ann Arbor, Michigan, USA). were found in the lungs of six snakes. The parasites Sequences of 28S and ITS genes of Rhabdiasidae were were fixed in hot 70% ethanol. For identification, the spe- retrieved from GenBank (table 3). As an outgroup the cimens were cleared with lactophenol on temporary taxon chosen was Rhabditoides regina (EF990726) for par- slides. The morphology was analysed using a computer- tial 28S. Sequences were aligned in ClustalX (Larkin ized system of image analysis (LAS DIC, Leica et al., 2007) using default settings and saved in FASTA for- Microsystems, Wetzlar, Germany). mat, Phylip format and NEXUS format. Two alignments The morphologies of tail, cuticle and oral structures were made, one with ITS (complete) and other with 28S were also evaluated by scanning electron microscopy (partial). The COI genes were not used, due to the small (SEM). Nematodes were fixed in 70% ethanol, dehydrated number of Rhabdiasidae sequences available in in a graded alcohol series and critically point dried. Then GenBank. The numbers of base substitutions per site be- they were mounted on an aluminium stub using conduct- tween sequences were calculated. Standard error esti- ive double-sided tape, coated with gold–palladium and mates were obtained by a bootstrap procedure (2000 examined with the use of a Quanta 200 scanning electron replicates). Analyses were conducted using the Kimura microscope (FEI Company; from Centro de Microscopia 2-parameter model; evolutionary analyses were con- Eletrônica de Botucatu, São Paulo, Brazil) (adapted from ducted in MEGA5 (Kimura, 1980; Tamura et al., 2011). Allison et al., 1972). The best-fit model for nucleotide substitution in the re- All measurements are reported in micrometres (μm) un- sulting matrix was TVM + I, determined by the Akaike in- less otherwise indicated. Data of the holotype are pre- formation criterion (AIC) in a jModelTest (Posada, 2008). sented in the text
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