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An integrative approach assesses the intraspecific variations of Procamallanus (Spirocamallanus) inopinatus, a common parasite in Neotropical freshwater fishes, and the phylogenetic patterns of Camallanidae

Published online by Cambridge University Press:  14 September 2020

Lorena G. Ailán-Choke ,
Luiz E.R. Tavares ,
José L. Luque  and
Felipe B. Pereira Open the ORCID record for Felipe B. Pereira [Opens in a new window]
Lorena G. Ailán-Choke
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Instituto para el Estudio de la Biodiversidad de Invertebrados, Facultad de Ciencias Naturales, Universidad Nacional de Salta, Av. Bolivia 5150, (4400) Salta, Argentina
Luiz E.R. Tavares
Affiliation:
Departamento de Patologia, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Av. Costa e Silva s/n°, CEP 79070-900, Campo Grande, MS, Brasil
José L. Luque
Affiliation:
Departamento de Parasitologia Animal, Instituto de Veterinária, Universidade Federal Rural do Rio de Janeiro, BR 465, Km 47, CEP 23851-970, Seropédica, RJ, Brasil
Felipe B. Pereira*
Affiliation:
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Presidente Antônio Carlos, 6627, Pampulha, CEP 31270-901, Belo Horizonte, MG, Brasil
*
Author for correspondence: Prof. Dr Felipe Bisaggio Pereira, E-mail: felipebisaggiop@hotmail.com
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Abstract

Integrative taxonomy was used to evaluate two component populations of Procamallanus (Spirocamallanus) inopinatus in Brazil and the phylogeny Camallanidae. Parasite populations were collected in the characiform Anostomoides passionis from River Xingu (Amazon basin) and Megaleporinus elongatus from River Miranda (Paraguay basin). Morphology was analysed using light and scanning electron microscopy (SEM). Genetic characterization was based on partial sequences of the 18S and 28S rDNA, and COI mtDNA. Phylogenies were based on 18S and COI due to data availability. Generalized Mixed Yule Coalescent (GMYC), Poisson Tree Process (PTP) and *BEAST were used for species delimitation and validation. SEM revealed for the first time the presence of minute denticles and pore-like structures surrounding the oral opening, phasmids in females and confirmed other important morphological aspects. Statistical comparison between the two-component populations indicated morphometric variations, especially among males. The different component population of P. (S.) inopinatus showed variable morphometry, but uniform morphology and were validated as conspecific by the GMYC, PTP and *BEAST. Some camallanid sequences in GenBank have incorrect taxonomic labelling. Host, environment and geographic aspects seem to be related to some lineages within Camallanidae; however, their real phylogenetic meanings are still unclear.

Keywords

AnostomidaeCharaciformesendoparasitehelminthintegrative taxonomymorphologyNematodagenetic characterization
Type
Research Article
Information
Parasitology , Volume 147 , Issue 14 , December 2020 , pp. 1752 - 1764
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Abdallah, VD, Azevedo, RK, Carvalho, ED and Silva, RJ (2012) New hosts and distribution records for nematode parasites of freshwater fishes from São Paulo State, Brazil. Neotropical Helminthology 6, 43–57.Google Scholar
Ailán-Choke, LG, Davies, DA, Tavares, LER. and Pereira, FB (2019) An integrative taxonomic assessment of Procamallanus (Spirocamallanus) huacraensis (Nematoda: camallanidae), infecting the freshwater catfish Trichomycterus spegazzinii (Siluriformes: Trichomycteridae) in Argentina. Parasitology Research 118, 2819–2829.10.1007/s00436-019-06429-0CrossRefGoogle Scholar
Albert, JS and Reis, RE (2011) Historical Biogeography of Neotropical Freshwater Fishes. Berkeley, CA: University of California Press.Google Scholar
Allio, R, Donega, S, Galtier, N and Nabholz, B. (2017) Large variation in the ratio of mitochondrial to nuclear rate across animals: implications for genetic diversity and the use of mitochondrial DNA as a molecular marker. Molecular Biology and Evolution 34, 2762–2772.10.1093/molbev/msx197CrossRefGoogle ScholarPubMed
Baele, G, Li, WS, Drummond, AJ, Suchard, MA and Lemey, P (2012) Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics. Molecular Biology and Evolution 30, 239–243.10.1093/molbev/mss243CrossRefGoogle ScholarPubMed
Bouckaert, R and Drummond, A (2017) Bmodeltest: Bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology 17, 42.10.1186/s12862-017-0890-6CrossRefGoogle ScholarPubMed
Bouckaert, R, Vaughan, TG, Barido-Sottani, J, Duchêne, S, Fourment, M, Gavryushkina, A, Heled, J, Jones, G, Kühnert, D, De Maio, N, Matschiner, M, Mendes, FK, Müller, NF, Ogilvie, HA, du Plessis, L, Popinga, A, Rambaut, A, Rasmussen, D, Siveroni, I, Suchard, MA, Wu, C-H., Xie, D, Zhang, C, Stadler, T and Drummond, AJ (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15, e1006650.10.1371/journal.pcbi.1006650CrossRefGoogle ScholarPubMed
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.10.2307/3284227CrossRefGoogle Scholar
Černotíková, E, Horák, A and Moravec, F (2011) Phylogenetic relationships of some spirurine nematodes (Nematoda: Chromadorea: Rhabditida: Spirurina) parasitic in fishes inferred from SSU rRNA gene sequences. Folia Parasitologica 58, 135–148.10.14411/fp.2011.013CrossRefGoogle ScholarPubMed
Chang, J-M, Di Tommaso, P and Notredame, C (2014) TCS: a new multiple sequence alignment reliability measure to estimate alignment accuracy and improve phylogenetic tree reconstruction. Molecular Biology and Evolution 31, 1625–1637.CrossRefGoogle ScholarPubMed
Chemes, SB and Takemoto, RM (2011) Diversity of parasites from middle Paraná system freshwater fishes, Argentina. International Journal of. Biodiversity and Conservation 3, 249–266.Google Scholar
Dagosta, FCP and Pinna, M (2017) Biogeography of Amazonian fishes: deconstructing river basins as biogeographic units. Neotropical Ichthyology 15, e170034.10.1590/1982-0224-20170034CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.10.1038/nmeth.2109CrossRefGoogle ScholarPubMed
Dohoo, I, Martin, W and Stryhn, H (2003) Veterinary Epidemiologic Research. Charlottetown: AVC Inc.Google Scholar
Froese, R and Pauly, D (eds) (2019) FishBase. World Wide Web electronic publication. http//www.fishbase.org (accessed 25 May 2020).Google Scholar
Frost, DR (2020) Amphibian Species of the World: an Online Reference. Version 6.1. World Wide Web electronic publication. https://amphibiansoftheworld.amnh.org/index.php. (accessed 25 august 2020). doi.org/10.5531/db.vz.0001.Google Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.10.1080/10635150390235520CrossRefGoogle ScholarPubMed
Heled, J and Drummond, AJ (2010) Bayesian Inference of species trees from multilocus data, Molecular Biology and Evolution 27, 570–580.10.1093/molbev/msp274CrossRefGoogle ScholarPubMed
Horton, T, Kroh, A, Ahyong, S, Bailly, N, Boyko, CB, Brandão, SN, Gofas, S, Hooper, JNA, Hernandez, F, Holovachov, O, Mees, J, Molodtsova, TN, Paulay, G, Decock, W, Dekeyzer, S, Poffyn, G, Vandepitte, L, Vanhoorne, B, Adlard, R, Agatha, S, Ahn, KJ, Akkari, N, Alvarez, B, Anderberg, A, Anderson, G, Angel, MV, Antic, D, Arango, C, Artois, T, Atkinson, S, Auffenberg, K, Baldwin, BG, Bank, R, Barber, A, Barbosa, JP, Bartsch, I, Bellan-Santini, D, Bergh, N, Bernot, J, Berta, A, Bezerra, TN, Bieler, R, Blanco, S, Blasco-Costa, I, Blazewicz, M, Bock, P, de León M, Bonifacino, Böttger-Schnack, R, Bouchet, P, Boury-Esnault, N, Boxshall, G, Bray, R, Bruce, NL, Cairns, S, Calvo Casas, J, Carballo, JL, Cárdenas, P, Carstens, E, Chan, BK, Chan, TY, Cheng, L, Churchill, M, Coleman, CO, Collins, AG, Collins, GE, Corbari, L, Cordeiro, R, Cornils, A, Coste, M, Costello, MJ, Crandall, KA, Cremonte, F, Cribb, T, Cutmore, S, Dahdouh-Guebas, F, Daly, M, Daneliya, M, Dauvin, JC, Davie, P, De Broyer, C, De Grave, S, de Mazancourt, V, de Voogd, NJ, Decker, P, Decraemer, W, Defaye, D, d'Hondt, JL, Dippenaar, S, Dohrmann, M, Dolan, J, Domning, D, Downey, R, Ector, L, Eisendle-Flöckner, U, Eitel, M, Encarnação, SCd, Enghoff, H, Epler, J, Ewers-Saucedo, C, Faber, M, Figueroa, D, Finn, J, Fišer, C, Fordyce, E, Foster, W, Frank, JH, Fransen, C, Freire, S, Furuya, H, Galea, H, Gao, T, Garcia-Alvarez, O, Garcia-Jacas, N, Garic, R, Garnett, S, Gasca, R, Gaviria-Melo, S, Gerken, S, Gibson, D, Gibson, R, Gil, J, Gittenberger, A, Glasby, C, Glover, A, Gómez-Noguera, SE, González-Solís, D, Gordon, D, Gostel, M, Grabowski, M, Gravili, C, Guerra-García, JM, Guidetti, R, Guiry, MD, Gutierrez, D, Hadfield, KA, Hajdu, E, Hallermann, J, Hayward, BW, Heiden, G, Hendrycks, E, Herbert, D, Herrera Bachiller, A, Js, Ho, Hodda, M, Høeg, J, Hoeksema, B, Houart, R, Hughes, L, Hyžný, M, Iniesta, LFM, Iseto, T, Ivanenko, S, Iwataki, M, Janssen, R, Jarms, G, Jaume, D, Jazdzewski, K, Jersabek, CD, Jóźwiak, P, Kabat, A, Kantor, Y, Karanovic, I, Karthick, B, Katinas, L, Kim, YH, King, R, Kirk, PM, Klautau, M, Kociolek, JP, Köhler, F, Kolb, J, Kotov, A, Kremenetskaia, A, Kristensen, RM, Kulikovskiy, M, Kullander, S, Kupriyanova, E, Lambert, G, Lazarus, D, Le Coze, F, LeCroy, S, Leduc, D, Lefkowitz, EJ, Lemaitre, R, Lichter-Marck, IH, Lindsay, D, Liu, Y, Loeuille, B, Lörz, AN, Lowry, J, Ludwig, T, Lundholm, N, Macpherson, E, Madin, L, Mah, C, Mamo, B, Mamos, T, Manconi, R, Mapstone, G, Marek, PE, Marshall, B, Marshall, DJ, Martin, P, Mast, R, McFadden, C, McInnes, SJ, Meidla, T, Meland, K, Merrin, KL, Messing, C, Mills, C, Moestrup, Ø, Mokievsky, V, Monniot, F, Mooi, R, Morandini, AC, Moreira da Rocha, R, Morrow, C, Mortelmans, J, Mortimer, J, Musco, L, Nesom, G, Neubauer, TA, Neubert, E, Neuhaus, B, Ng, P, Nguyen, AD, Nielsen, C, Nishikawa, T, Norenburg, J, O'Hara, T, Opresko, D, Osawa, M, Osigus, HJ, Ota, Y, Páll-Gergely, B, Panero, JL, Pasini, E, Patterson, D, Paxton, H, Pelser, P, Peña-Santiago, R, Perrier, V, Perrin, W, Petrescu, I, Picton, B, Pilger, JF, Pisera, AB, Polhemus, D, Poore, GC, Potapova, M, Pugh, P, Read, G, Reich, M, Reimer, JD, Reip, H, Reuscher, M, Reynolds, JW, Richling, I, Rimet, F, Ríos, P, Rius, M, Rodríguez, E, Rogers, DC, Roque, N, Rosenberg, G, Rützler, K, Sabbe, K, Saiz-Salinas, J, Sala, S, Santagata, S, Santos, S, Sar, E, Satoh, A, Saucède, T, Schatz, H, Schierwater, B, Schilling, E, Schmidt-Rhaesa, A, Schneider, S, Schönberg, C, Schuchert, P, Senna, AR, Serejo, C, Shaik, S, Shamsi, S, Sharma, J, Shear, WA, Shenkar, N, Shinn, A, Short, M, Sicinski, J, Sierwald, P, Simmons, E, Sinniger, F, Sivell, D, Sket, B, Smit, H, Smit, N, Smol, N, Souza-Filho, JF, Spelda, J, Sterrer, W, Stienen, E, Stoev, P, Stöhr, S, Strand, M, Suárez-Morales, E, Summers, M, Suppan, L, Susanna, A, Suttle, C, Swalla, BJ, Taiti, S, Tanaka, M, Tandberg, AH, Tang, D, Tasker, M, Taylor, J, Taylor, J, Tchesunov, A, Temereva, E, ten Hove, H, ter Poorten, JJ, Thomas, JD, Thuesen, EV, Thurston, M, Thuy, B, Timi, JT, Timm, T, Todaro, A, Turon, X, Tyler, S, Uetz, P, Urbatsch, L, Uribe-Palomino, J, Urtubey, E, Utevsky, S, Vacelet, J, Vachard, D, Vader, W, Väinölä, R, Van de Vijver, B, van der Meij, SE, van Haaren, T, van Soest, RW, Vanreusel, A, Venekey, V, Vinarski, M, Vonk, R, Vos, C, Walker-Smith, G, Walter, TC, Watling, L, Wayland, M, Wesener, T, Wetzel, CE, Whipps, C, White, K, Wieneke, U, Williams, DM, Williams, G, Wilson, R, Witkowski, A, Witkowski, J, Wyatt, N, Wylezich, C, Xu, K, Zanol, J, Zeidler, W and Zhao, Z (2020) World Register of Marine Species. World Wide Web electronic publication. https://www.marinespecies.org (accessed 25 august 2020). https://doi.org/10.14284/170.Google Scholar
Huelsenbeck, JP and Ronquist, F (2001) Mrbayes: Bayesian inference of phylogenetic trees. Bioinformatics (Oxford, England) 17, 754–755.10.1093/bioinformatics/17.8.754CrossRefGoogle ScholarPubMed
Iannacone, JA, López, EN and Alvariño, LF (2000) Procamallanus (Spirocamallanus) inopinatus Travassos, Artigas et Pereira, 1928 (Nematoda: Camallanidae) parásito de Triportheus angulatus (Spix, 1829) (Characidae) en la laguna de Yarinacocha, Ucayali-Peru. Biologia Pesquera 28, 37–43.Google Scholar
Jackson, JA and Tinsle, RC (1995) Representatives of Batrachocamallanus N. g. (Nematoda: Procamallaninae) from Xenopus Spp. (Anura: Pipidae): geographical distribution, host range and evolutionary relationships. Systematic Parasitology 31, 159–188.10.1007/BF00009115CrossRefGoogle Scholar
Kimura, M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 1l1–120.Google ScholarPubMed
Kloss, GR (1966) Helmintos parasitos de espécies simpátricas de Astyanax (Pisces, Characidae). Papéis Avulsos do Departamento de Zoologia São Paulo 18, 189–219.Google Scholar
Kohn, A and Fernandes, BMM (1987) Estudo comparativo dos helmintos parasitos de peixes do Rio Mogi Guassu, coletados nas excursões realizadas entre 1927 e 1985. Memórias do Instituto Oswaldo Cruz 82, 483–500.10.1590/S0074-02761987000400006CrossRefGoogle Scholar
Luque, JL, Aguiar, JC, Vieira, FM, Gibson, DI and Portes-Santos, C (2011) Checklist of Nematoda associated with the fishes of Brazil. Zootaxa 3082, 1–88.10.11646/zootaxa.3082.1.1CrossRefGoogle Scholar
Luque, JL, Cruces, C, Chero, J, Paschoal, F, Alves, PV, Da Silva, AC, Sanchez, L and Iannacone, J (2016) Checklist of metazoan parasites of fishes from Peru. Check List (Luis Felipe Toledo) 6, 659–667.Google Scholar
Moravec, F (1998) Nematodes of Freshwater Fishes of the Neotropical Region. Praha: Academia.Google Scholar
Moravec, F and Jirků, M (2015) Two Procamallanus (Spirocamallanus) species (Nematoda: Camallanidae) from freshwater fishes in lower Congo river. Acta Parasitologica 60, 226–233.10.1515/ap-2015-0032CrossRefGoogle ScholarPubMed
Moravec, F and Justine, J-L. (2019) A new species and new records of camallanid nematodes (Nematoda, Camallanidae) from marine fishes and seas snakes in New Caledonia. Parasite 26, 66.10.1051/parasite/2019068CrossRefGoogle ScholarPubMed
Moravec, F and Thatcher, VE (1997) Procamallanus (Denticamallanus Subgen. n.) dentatus sp. n. (Nematoda, Camallanidae) from the characid fish, Bryconops Alburnoides, in the Brazilian Amazon. Parasite 4, 239–243.10.1051/parasite/1997043239CrossRefGoogle Scholar
Moravec, F, Kohn, A and Fernandes, BMM (1993) Nematode parasites of fishes of the Paraná River, Brazil. Part 3. Camallanoidea and Dracunculoidea. Folia Parasitologica 40, 211–229.Google Scholar
Moravec, F, Prouza, A and Royero, R (1997) Some nematodes of freshwater fishes in Venezuela. Folia Parasitologica 44, 33–47.Google ScholarPubMed
Moravec, F, Salgado-Maldonado, G and Caspeta-Mandujano, J (2000) Three new Procamallanus (Spirocamallanus) species from freshwater fishes in Mexico. Journal of Parasitology 86, 119–127.10.1645/0022-3395(2000)086[0119:TNPSSF]2.0.CO;2CrossRefGoogle ScholarPubMed
Moravec, F, Justine, J-L, Würtz, J, Tarachewski, H and Sasal, P (2006) A new species of Procamallanus (Nematoda: Camallanidae) from Pacific eels (Anguilla Spp.). Journal of Parasitology 92, 130–137.10.1645/GE-3509.1CrossRefGoogle Scholar
Moreira, NIB., Oliveira, CL and Costa, HMA (1994) Spirocamallanus inopinatus (Travassos, Artigas & Pereira, 1928) e Spirocamallanus Saofranciscencis sp. n. (Nematoda, Camallanidae) em peixes da Represa de Tres Maria. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 46, 485–500.Google Scholar
Nichols, R (2001) Gene trees and species trees are not the same. Trends in Ecology and Evolution 16, 358–364.10.1016/S0169-5347(01)02203-0CrossRefGoogle Scholar
Notredame, C, Higgins, DG and Heringa, J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. Journal of Molecular Biology 302, 205–217.10.1006/jmbi.2000.4042CrossRefGoogle ScholarPubMed
Pereira, C (1935) Ascaridata e spirurata parasitos de peixes do Nordeste Brasileiro. Arquivos do Instituto Biológico São Paulo 6, 53–62.Google Scholar
Petter, AJ and Dlouhy, C (1985) Nématodes de Poissons du Paraguay. III. Camallanina. Description d'une espèce et d'une sous-espèce nouvelles de la famille des Guyanemidae. Revue Suisse de Zoologie 92, 165–175.10.5962/bhl.part.81607CrossRefGoogle Scholar
Petter, AJ and Thatcher, VE (1988) Observations sur la structure de la capsule buccale de Spirocamallanus inopinatus (Nematoda), parasite de poissons brésiliens. Bulletin du Museum National d'Histoire Naturelle 10, 685–692.Google Scholar
Pinheiro, RH da, S, Melo, FTV, Monks, S, dos Santos, JN and Giese, EG (2018) A new species of Procamallanus Baylis, 1923 (Nematoda, camallanidae) from Astronotus ocellatus (Agassiz, 1831) (Perciformes, Cichlidae) in Brazil. Zookeys 790, 21–33.10.3897/zookeys.790.24745CrossRefGoogle Scholar
Pons, J, Barraclough, TG, Gomez-Zurita, J, Cardoso, A, Duran, DP, Hazell, S, Kamoun, S, Sumlin, WD and Vogler, AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.10.1080/10635150600852011CrossRefGoogle ScholarPubMed
Puillandre, N, Lambert, A, Brouillet, S and Achaz, G (2012) ABGD, automatic barcode Gap discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.10.1111/j.1365-294X.2011.05239.xCrossRefGoogle ScholarPubMed
Rambaut, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using tracer 1.7. Systematic Biology 67, 901–904. https://doi.org/10.1093/sysbio/syy032 .CrossRefGoogle ScholarPubMed
Razkin, O, Sonet, G, Breugelmans, K, Madeira, MJ, Gómez-Moliner, BJ and Backeljau, T (2016) Species limits, interspecific hybridization and phylogeny in the cryptic land snail complex Pyramidula: the power of RADseq data. Molecular Phylogenetics and Evolution 101, 267–278.10.1016/j.ympev.2016.05.002CrossRefGoogle ScholarPubMed
Reis, RE, Albert, JS, Di Dario, F, Mincarones, MM, Petry, P and Rocha, LA (2016) Fish biodiversity and conservation in South America. Journal of Fish Biology 89, 12–47.10.1111/jfb.13016CrossRefGoogle Scholar
Sardella, CJ, Pereira, FB and Luque, JL (2017) Redescription and first genetic characterisation of Procamallanus (Spirocamallanus) Macaensis Vicente & Santos, 1972 (Nematoda: Camallanidae), including re-evaluation of the species of Procamallanus (Spirocamallanus) from marine fishes off Brazil. Systematic Parasitology 94, 657–668.10.1007/s11230-017-9728-2CrossRefGoogle ScholarPubMed
Svitin, R, Schoeman, AL 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 Parasitologica 65, 003.10.14411/fp.2018.003CrossRefGoogle ScholarPubMed
Svitin, R, Truter, M, Kudlai, O, Smit, NJ and du Preez, L. (2019) Novel information on the morphology, phylogeny and distribution of camallanid nematodes from marine and freshwater hosts in South Africa, including the description of Camallanus Sodwanaensis n. sp. International Journal for Parasitology: Parasites and Wildlife 10, 263–273.Google ScholarPubMed
Townsend, JP (2007) Profiling phylogenetic informativeness. Systematic Biology 56, 222–231.10.1080/10635150701311362CrossRefGoogle ScholarPubMed
Travassos, L, Artigas, P and Pereira, C (1928) Fauna helmintológica dos peixes de água doce do Brasil. Arquivos do Instituto Biológico 1, 5–68.Google Scholar
Uetz, P, Freed, P and Hosek, J (eds) (2020) The Reptile Database. World Wide Web electronic publication. http://www.reptile-database.org (accessed 25 May 2020).Google Scholar
Vicentin, W, Vieira, KRI, Tavares, LER., Costa, FE, Takemoto, RM and Paiva, F (2013) Metazoan endoparasites of Pygocentrus Nattereri (Characiformes: Serrasalminae) in the Negro river, Pantanal, Brazil. Revista Brasileira de Parasitologia Veterinária 22, 331–338.10.1590/S1984-29612013000300003CrossRefGoogle ScholarPubMed
Wijová, M, Moravec, F, Horák, A and Lukeš, J (2006) Evolutionary relationships of Spirurina (Nematoda: Chromadorea: Rhabditida) with special emphasis on dracunculoid nematodes inferred from SSU rRNA gene sequences. International Journal for Parasitology 36, 1067–1075.10.1016/j.ijpara.2006.04.005CrossRefGoogle ScholarPubMed
Xia, X (2018) DAMBE 7: new and improved tools for data analysis in molecular biology and evolution. Molecular Biology and Evolution 35, 1550–1552.10.1093/molbev/msy073CrossRefGoogle Scholar
Xia, X, Xie, Z and Li, WH (2003) Effects of GC content and mutational pressure on the lengths of exons and coding sequences. Journal of Molecular Evolution 56, 362–370.10.1007/s00239-002-2406-1CrossRefGoogle ScholarPubMed
Zar, JH (2010) Biostatistical Analysis. Englewood Cliffs: Prentice Hall.Google Scholar
Zhang, J, Kapli, P, Pavlidis, P and Stamatakis, A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics (Oxford, England) 29, 2869–2876.CrossRefGoogle ScholarPubMed
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