Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-28T03:47:17.800Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological and genetic characterization of Pterygodermatites (Paucipectines) zygodontomis (Nematoda: Rictulariidae) from Necromys lasiurus (Rodentia: Sigmodontinae) from Uberlândia, Brazil

Published online by Cambridge University Press:  04 October 2017

N.A. Costa ,
R.O. Simões ,
R.V. Vilela ,
J.G.R. Souza ,
S.T. Cardoso ,
N.O. Leiner ,
R. Gentile  and
A. Maldonado Junior
N.A. Costa
Affiliation:
Programa de Pós-Graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21040-360, Brasil Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21040-360, Brasil
R.O. Simões
Affiliation:
Programa de Pós-Graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21040-360, Brasil Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21040-360, Brasil
R.V. Vilela
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21040-360, Brasil
J.G.R. Souza
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21040-360, Brasil
S.T. Cardoso
Affiliation:
Programa de Pós-Graduação em Ecologia e Conservação dos Recursos Naturais, Instituto de Biologia, Universidade Federal de Uberlândia, Rua Ceará s/n, Uberlândia, MG, 38405-315, Brasil Laboratório de Ecologia de Mamíferos, Instituto de Biologia, Universidade Federal de Uberlândia, Rua Ceará s/n, Uberlândia, MG, 38405-315, Brasil
N.O. Leiner
Affiliation:
Laboratório de Ecologia de Mamíferos, Instituto de Biologia, Universidade Federal de Uberlândia, Rua Ceará s/n, Uberlândia, MG, 38405-315, Brasil
R. Gentile
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21040-360, Brasil
A. Maldonado Junior*
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil 4365, Rio de Janeiro, RJ, 21040-360, Brasil
*
Author for correspondence: A. Maldonado, E-mail: maldonad@ioc.fiocruz.br
Get access Rights & Permissions [Opens in a new window]

Abstract

Pterygodermatites (Paucipectines) zygodontomis, a nematode parasite of the small intestine of the rodent Necromys lasiurus, from Uberlândia, Minas Gerais state, Brazil, was analysed by light and scanning electron microscopy. Additionally, phylogenies were inferred from the mitochondrially encoded cytochrome c oxidase I gene (MT-CO1). Details of the helminth surface, such as the oral aperture, cephalic papillae, papillae in the posterior region of the body and longitudinal cuticular elements represented by spine-like projections and fans are presented, adding new taxonomic details. Molecular phylogenetic analysis, based on the MT-CO1, demonstrated that P. (P.) zygodontomis and Pterygodermatites (Paucipectines) jaegerskioldi form a unique evolutionary unit in accordance with the subgenus Paucipectines and corroborated their occurrence in cricetid and didelphid hosts.

Type
Research Paper
Information
Journal of Helminthology , Volume 92 , Issue 5 , September 2018 , pp. 618 - 629
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the nematode parasites of vertebrates. 463 pp. Wallingford, CABI.Google Scholar
Blaxter, ML, De Ley, P, Garey, JR, Liu, LX, Scheldeman, P, Vierstraete, A and Vida, JT (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–75.Google Scholar
Bonvicino, C.R, Oliveira, JA and D'Andrea, PS (2008) Guia dos Roedores do Brasil, com chavez para gêneros baseadas em caracteres externos. 120pp. Rio de Janeiro, Centro Pan-Americano de Febre Aftosa – OPAS/OMS.Google Scholar
Brandão-Filho, SP, Brito, M.E, Carvalho, FG, Ishikawa, EA, Cupolillo, E, Floeter-Winter, L and Shaw, JJ (2003) Wild and synantrophic hosts of Leshmania (Viannia) braziliensis in the endemic cutaneous leishmaniasis locality of Amaraji, Pernambuco State, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 37, 291–296.Google Scholar
Cardoso, TS, Simões, RO, Luque, JLF, Maldonado, A and Gentile, R (2016) The influence of habitat fragmentation on helminth communities in rodent populations from a Brazilian Mountain Atlantic Forest. Journal of Helminthology 90, 460–468.Google Scholar
Carmignotto, AP, de Vivo, M and Langguth, A (2012) Mammals of the Cerrado and Caatinga: distribution patterns of the tropical open biomes of Central South America. pp. 307–350 in Patterson, BD and Costa, LP (Eds) Bones, clones, and biomes: the history and geography of recent Neotropical mammals. Chicago, University of Chicago Press.Google Scholar
Casiraghi, M, Anderson, TJ, Bandi, C, Bazzocchi, C and Genchi, C (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122, 93–103.Google Scholar
Chabaud, AG and Bain, O (1981) Quentius kozeki n. g., n. sp., Nématode rictulaire parasite d'um Marsupial américain. Annales de Parasitologie 56, 175–178.Google Scholar
Chaudhary, A, Verma, C, Tomar, V and Singh, HS (2017) Procamallanus spiculogubernaculus Agarwal, 1958 (Nematoda: Camallanidae) from Stinging catfish, Heteropneustes fossilis in India: morphological characterization and molecular data. Helminthologia 54, 1–9.Google Scholar
Crainey, JL, da Silva, TRR, Encinas, F, Marín, MA, Vicente, ACP and Luz, SLB (2016) The mitogenome of Onchocerca volvulus from the Brazilian Amazonia focus. Memórias do Instituto Oswaldo Cruz 111, 79–81.Google Scholar
D'Elia, G (2003) Phylogenetics of Sigmodontinae (Rodentia, Muroidea, Cricetidae), with special reference to the Akodont group and with additional comments on historical biogeography. Cladistics 19, 307–323.Google Scholar
Ferguson, J.A, Woodberry, K, Gillin, CM, Jackson, DH, Sanders, JL, Madigan, W, Bildfell, RJ and Kent, ML (2011) Cylicospirura species (Nematoda: Spirocercidae) and stomach nodules in cougars (Puma concolor) and bobcats (Lynx rufus) in Oregon. Journal of Wildlife Diseases 47, 140–153.Google Scholar
Francisco, AL, Magnusson, WE and Sanaiotti, TM (1995) Variation growth and reproduction of Bolomys lasiurus (Rodentia: Muridae) in an Amazonian Savanna. Journal of Tropical Ecology 11, 419–428.Google Scholar
Gardner, SL and Campbell, MI (1992) Parasites as probes for biodiversity. Journal of Parasitology 78, 596–600.Google Scholar
Gentile, R, Costa Neto, SF and D'Andrea, PS (2010) Uma revisão sobre a participação do rato d'água Nectomys squamipes na dinâmica de transmissão da esquistossomose mansônica: Um estudo multidisciplinar de longo prazo em uma área endêmica. Oecologia Australis 14, 711–725.Google Scholar
Ghedin, E, Wang, S, Spiro, D, et al. (2007) Draft genome of the filarial nematode parasite Brugia malayi. Science 80, 1756–1760.Google Scholar
Grenfell, BT (1992) Parasitism and the dynamics of ungulate grazing systems. American Naturalist 139, 907–929.Google Scholar
Grossmann, NV (2015) Relações Parasito-Hospedeiro de Endo e Ectoparasitas em Pequenos Mamíferos em um Cerrado do Brasil Central. 167 pp. Brasília, Universidade de Brasília, Instituto de Ciências Biológicas.Google Scholar
Hodda, M (2011) Phylum Nematoda Cobb 1932. pp. 63–95 in Zhang, Z.-Q. (Ed.) Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Auckland, NZ, Magnolia Press.Google Scholar
Iorio, R, Šlapeta, J, Otranto, D, Paoletti, B, Giangaspero, A and Traversa, D (2009) Phylogenetic relationships of Habronema microstoma and Habronema muscae (Spirurida: Habronematidae) within the order Spirurida inferred using mitochondrial cytochrome c oxidase subunit 1 (cox1) gene analysis. Parasitological Research 104, 979–984.Google Scholar
Jiménez, FA and Patterson, BD (2012) A new species of Pterygodermatites (Nematoda: Rictulariidae) from the Incan shrew opossum, Lestoros inca. Journal of Parasitology 98, 604–607.Google Scholar
Jobb, G. (2011) TREEFINDER version of March 2011. Munich. Distributed by the author at www.treefinder.de (accessed 16 August 2015).Google Scholar
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Mentjies, P and Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.Google Scholar
Kim, J, Kern, E, Kim, T, Sim, M, Kim, J, Kim, Y, Park, C, Nadler, SA and Park, JK (2017) Phylogenetic analysis of two Plectus mitochondrial genomes (Nematoda: Plectida) supports a sister group relationship between Plectida and Rhabditida within Chromadorea. Molecular Phylogenetics and Evolution 107, 90–102.Google Scholar
Lefoulon, E, Bain, O, Bourret, J, Junker, K, Guerrero, R, Cañizales, I, Kuzmin, Y, Satoto, TBT, Cardenas-Callirgos, JM, de Souza Lima, S, Raccurt, C, Mutafchiev, Y, Gavotte, L and Martin, C (2015) Shaking the tree: multi-locus sequence typing usurps current Onchocercid (filarial nematode) phylogeny. PLoS Neglected Tropical Diseases 9, 1–19.Google Scholar
Lemos, ERS and D'Andrea, PS (2014) Trabalho com animais silvestres: procedimentos, riscos e biossegurança. 180 pp. Rio de Janeiro, Editora Fiocruz.Google Scholar
Lent, H and Freitas, JF (1935) Sobre dois novos nematódeos parasitos de quica: Caluromys philander. Memórias do Instituto Oswaldo Cruz 30, 535–542.Google Scholar
Ley, P and Blaxter, ML (2002) Systematic position and phylogeny. pp. 1–30 in Lee, D (Ed.) The biology of nematodes. London, Taylor & Francis.Google Scholar
Lichtenfels, JR (1970) Two new species of Pterygodermatites (Paucipectines) Quentin, 1969 (Nematoda: Rictulariidae) with a key to the species from North American rodents. Proceedings of the Helminthological Society of Washington 37, 94–101.Google Scholar
Limongi, JE, Moreira, FG, Peres, JB, Suzuki, A, Ferreira, IB, Souza, RP, Pinto, RMC and Pereira, LE (2013) Serological survey of hantavirus in rodents in Uberlândia, Minas Gerais, Brazil. Revista Instituto de Medicina Tropical 55, 155–158.Google Scholar
Liu, GH, Gasser, RB, Otranto, D, Xu, MJ, Shen, JL, Mohandas, N, Zhou, DH and Zhu, XQ (2013a) Mitochondrial genome of the eyeworm, Thelazia callipaeda (Nematoda: Spirurida), as the first representative from the family Thelaziidae. PLoS Neglected Tropical Diseases 7, e2029.Google Scholar
Liu, GH, Wang, Y, Song, HQ, Li, MW, Ai, L, Yu, XL and Zhu, XQ (2013b) Characterization of the complete mitochondrial genome of Spirocerca lupi: sequence, gene organization and phylogenetic implications. Parasites & Vectors 6, 45–54.Google Scholar
Liu, GH, Jia, YQ, Wang, YN, Zhao, GH and Zhu, XQ (2015a) The complete mitochondrial genome of the gullet worm Gongylonema pulchrum: gene content, arrangement, composition and phylogenetic implications. Parasites & Vectors 8, 1–8.Google Scholar
Liu, GH, Shao, R, Cai, XQ, Li, WW and Zhu, XQ (2015b) Gnathostoma spinigerum mitochondrial genome sequence: a novel gene arrangement and its phylogenetic position within the class Chromadorea. Scientific Reports 5, 12691.Google Scholar
Liu, GH, Li, JY and Zhu, XQ (2017) Characterization of the complete mitochondrial genome of Setaria digitata (Nematoda: Setariidae) from China. Journal of Helminthology, 1–5. doi:10.1017/S0022149X16000912.Google Scholar
Lynggaard, C, García-Prieto, L, Guzmán-Cornejo, C and Osorio-Sarabia, D (2014) Pterygodermatites (Paucipectines) baiomydis n. sp. (Nematoda: Rictulariidae), a parasite of Baiomys taylori (Cricetidae). Parasite 21, 58.Google Scholar
Mafra, AC and Lanfredi, RM (1998) Reevaluation of Physaloptera bispiculata (Nematoda: Spiruroidaea) by light and scanning electron microscopy. Journal of Parasitology 84, 582–588.Google Scholar
McNulty, SN, Mullin, AS, Vaughan, JA, Tkach, V.V, Weil, GJ and Fischer, PU (2012) Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species. BMC Genomics 13, 145–155.Google Scholar
Miño, MH, Rojas Herrera, EJ, Notarnicola, J, Robles, MR and Navone, GT (2012) Diversity of the helminth community of the Pampean grassland mouse (Akodon azarae) on poultry farms in central Argentina. Journal of Helminthology 86, 46–53.Google Scholar
Morand, S and Arias-Gonzalez, E (1997) Is parasitism a missing ingredient in model ecosystems? Ecological Modeling 95, 61–74.Google Scholar
Morand, S, Ivanova, ES and Vaucher, C (1996) Dicelis keymeri n. sp. (Nematoda: Drilonematidae) from the earthworm Octalasium pseudotranspadanum Zicsi. Proceedings of the Helminthological Society of Washington 63, 19–23.Google Scholar
Moreira, VLC, Giese, EG, Melo, FTV, Simões, RO, Thiengo, SC, Maldonado, A Jr and Santos, JN (2013) Endemic angiostrongyliasis in the Brazilian Amazon: natural parasitism of Angiostrongylus cantonensis in Rattus rattus and R. norvegicus and sympatric giant African land snails, Achatina fulica. Acta Tropica 125, 90–97.Google Scholar
Mutafchiev, Y, Mariaux, J and Georgiev, BB (2014) Description of Proyseria petterae n. sp., with an amended generic diagnosis and a review of the species of Proyseria Petter, 1959 and Stegophorus Wehr, 1934 (Nematoda: Acuariidae). Systematic Parasitology 89, 3–14.Google Scholar
Mutafchiev, Y, Mariaux, J and Georgiev, BB (2017) Description of Acuaria europaea n. sp. (Spirurida: Acuariidae) from Dendrocopos syriacus (Hemprich & Ehrenberg) and Oriolus oriolus (L.) (Aves) in Europe, with results of re-examination of related European species of Acuaria Bremser, 1811. Systematic Parasitology 94, 201–214.Google Scholar
Nadler, SA, Carreno, RA, Mejía-Madrid, H, Ullberg, J, Pagan, C, Houston, R and Hugot, JP (2007) Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology 134, 1421–1442.Google Scholar
Navone, GT (1989) Pterygodermatites (Paucipectines) kozeki (Chabaud et Bain, 1981) n. comb., parásito de Lestodelphys halli Tate, 1934, Didelphis albiventris L. y Thylamis pusilla (Desmarest) de la República Argentina. Anatomía y posición sistemática. Revista Ibérica de Parasitología 49, 219–226.Google Scholar
Navone, GT and Suriano, DM (1992) Pterigodermatites (Paucipectines) spinicaudatis n. sp. (Nematoda: Rictularidae) from Dromiciops australis (Marsupialia: Microbiotheriidae) in Bariloche, Rio Negro, Argentina. Biogeographical distribution and host–parasite relationships. Memórias do Instituto Oswaldo Cruz 87, 533–538.Google Scholar
Oliveira, RC, Guterres, A, Fernandes, J, D'Andrea, PS, Bonvicino, CR and de Lemos, ERS (2014) Hantavirus reservoirs: current status with an emphasis on data from Brazil. Viruses 6, 1929–1973.Google Scholar
Orozco, MM, Piccinali, RV, Mora, MS, Enriquez, GF, Cardinal, MV and Gürtler, RE (2014) The role of sigmodontine rodents as sylvatic hosts of Trypanosoma cruzi in the Argentinean Chaco. Infection Genetics and Evolution 22, 12–22.Google Scholar
Pinotti, BT, Naxara, L and Pardini, R (2011) Diet and food selection by small mammals in an old-growth Atlantic forest of south-eastern Brazil. Studies on Neotropical Fauna and Environment 46, 1–9.Google Scholar
Poulin, R (1998) Comparison of three estimators of species richness in parasite component communities. Journal of Parasitology 84, 485–490.Google Scholar
Prosser, SWJ, Velarde-Aguilar, MG, León-Règagnon, V and Hebert, PDN (2013) Advancing nematode barcoding: a primer cocktail for the cytochrome c oxidase subunit I gene from vertebrate parasitic nematodes. Molecular Ecology Resources 13, 1108–1115.Google Scholar
Quentin, JC (1967) Rictularia zygodontomis n. sp., nématode nouveau parasite de rongeurs Du Brésil. Bulletin du Muséum National D'Histoire Naturelle, Paris 39, 740–744.Google Scholar
Quentin, JC (1969) Essai de classification des nématodes rictulaires. Mémoires du Muséum National D'histoire Naturalle LIV, 1–115.Google Scholar
Ramallo, G and Claps, LE (2007) Nuevos hospedadores y registros geograficos de Pterygodermatites (Paucipectines) kozeki (Nematoda, Rictulariidae) en Argentina. Mastozoología Neotropical 14, 93–96.Google Scholar
Rambaut, A (2012) FigTree, a graphical viewer of phylogenetic trees. Available at http://tree.bio.ed.ac.uk/software/figtree (accessed 5 May 2017).Google Scholar
Ramesh, A, Small, ST, Kloos, ZA, Kazura, JW, Nutman, TB, Serre, D and Zimmerman, PA (2012) The complete mitochondrial genome sequence of the filarial nematode Wuchereria bancrofti from three geographic isolates provides evidence of complex demographic history. Molecular and Biochemical Parasitology 183, 32–41.Google Scholar
Redford, K and Eisenberg, J (1999) Mammals of the Neotropics. 3rd edn. 624 pp. Chicago, The University of Chicago Press.Google Scholar
Ronquist, F, Teslenko, M, van derMark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542Google Scholar
Sabino-Santos, G, Maia, FGM, Jonsson, CB, Goodin, DG, Salazar-Bravo, J and Figueiredo, LTM (2016) Serologic evidence of mammarenaviruses among wild rodents in Brazil. Journal of Wildlife Diseases 52, 766–769.Google Scholar
Schwarz, G (1978) Estimating the dimension of a model. Institute of Mathematical Statistics. Annals of Statistics 6, 461–464.Google Scholar
Setsuda, A, Da, N, Hasegawa, H, Behnke, JM, Rana, HB, Dhakal, IP and Sato, H (2016) Intraspecific and interspecific genetic variation of Gongylonema pulchrum and two rodent Gongylonema spp. (G. aegypti and G. neoplasticum), with the proposal of G. nepalensis n. sp. for the isolate in water buffaloes from Nepal. Parasitological Research 115, 787–795.Google Scholar
Simões, R, Gentile, R, Rademaker, V, D'Andrea, P, Herrera, H, Freitas, T, Lanfredi, R and Maldonado, A (2010) Variation in the helminth community structure of Thrichomys pachyurus (Rodentia: Echimyidae) in two sub-regions of the Brazilian Pantanal: the effects of land use and seasonality. Journal of Helminthology 84, 266–275.Google Scholar
Smales, LR, Harris, PD and Behnke, JM (2009) A redescription of Protospirura muricola Gedoelst, 1916 (Nematoda: Spiruridae), a parasite of murid rodents. Systematic Parasitology 72, 15–26.Google Scholar
Su, YB, Kong, SC, Wang, LX, Chen, L and Fang, R (2016) Complete mitochondrial genome of Philometra carassii (Nematoda: Philometridae). Mitochondrial DNA. Part A, DNA mapping, sequencing, and analysis 27, 1397–1398.Google Scholar
Sun, MM, Ma, J, Sugiyama, H, Ando, K, Li, WW, Xu, QM, Liu, GH and Zhu, XQ (2016) The complete mitochondrial genomes of Gnathostoma doloresi from China and Japan. Parasitological Research 115, 4013–4020.Google Scholar
Sun, MM, Liu, GH, Ando, K, Woo, HC, Ma, J, Sohn, WM, Sugiyama, H and Zhu, XQ (2017) Complete mitochondrial genomes of Gnathostoma nipponicum and Gnathostoma sp., and their comparison with other Gnathostoma species. Infection, Genetics and Evolution 48, 109–115.Google Scholar
Sutton, CA (1979) Contribución al conocimiento de la fauna parasitológica Argentina. IV. Rictularia massoiai sp. n. y Enterobius yagoi sp. n. (Nematoda). Acta Zoologica Lilloana 35, 29–37.Google Scholar
Sutton, CA (1984) Contribución al conocimiento de la fauna parasitológica Argentina XIII Nuevos nematodes de la familia Rictulariidae. Neotropica 30, 141–152.Google Scholar
Talamoni, SA, Couto, D, Cordeiro, DA Júnior and Diniz, FM (2008) Diet of some species of Neotropical small mammals. Mammalian Biology 73, 337–341.Google Scholar
Thomas, F, Renaud, F and Guégan, JF (2005) Parasitism and ecosystems. 229 pp. New York, Oxford University Press.Google Scholar
Torres, EL, Maldonado, A Jr and Lanfredi, RM (2007) Pterygodermatites (Paucipectines) jägerskiöldi (Nematoda: Rictulariidae) from Gracilinanus agilis and G. microtarsus (Marsupialia: Didelphidae) in Brazilian Pantanal and Atlantic Forest by light and scanning electron microscopy. Journal of Parasitology 93, 274–279.Google Scholar
Vicente, JJ, Rodrigues, HO, Gomes, DC and Pinto, RM (1997) Nematoides do Brasil. Parte V: Nematóides de Mamíferos. Revista Brasileira de Zoologia 14(Suppl. 1), 1–452.Google Scholar
Vieira, EM and Baumgarten, LC (1995) Daily activity patterns of small mammals in a Cerrado Area from central Brazil. Journal of Tropical Ecology 11, 255–262.Google Scholar
Wijová, M, Moravec, F, Horak, A, Modry, D and Lukes, J (2005) Phylogenetic position of Dracunculus medinensis and some related nematodes inferred from 18S rRNA. Parasitology Research 96, 133–135.Google Scholar
Xia, X (2017) DAMBE6: New tools for microbial genomics, phylogenetics and molecular evolution. Journal of Heredity 108, 431–437.Google Scholar
Xia, X and Lemey, P (2009) Assessing substitution saturation with DAMBE. pp. 615–630 in Lemey, P, Salemi, M and Vandamme, AM (Eds) The phylogenetic handbook: A practical approach to DNA and protein phylogeny. 2nd edn. Cambridge, Cambridge University Press.Google Scholar
Xia, X, Xie, Z, Salemi, M, Chen, L and Wang, Y (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1–7.Google Scholar
Supplementary material: File

Costa et al supplementary material

Costa et al supplementary material 1

Download Costa et al supplementary material(File)
File 21.9 KB