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A new species of Physaloptera (Nematoda: Spirurida) from Proechimys gardneri (Rodentia: Echimyidae) from the Amazon rainforest and molecular phylogenetic analyses of the genus

Published online by Cambridge University Press:  24 July 2019

A. Maldonado Jr ,
R.O. Simões Open the ORCID record for R.O. Simões [Opens in a new window] ,
J. São Luiz ,
S.F. Costa-Neto  and
R.V. Vilela
A. Maldonado Jr
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, FIOCRUZ, Rio de Janeiro, RJ, Brazil
R.O. Simões*
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, FIOCRUZ, Rio de Janeiro, RJ, Brazil Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, Brazil
J. São Luiz
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, FIOCRUZ, Rio de Janeiro, RJ, Brazil
S.F. Costa-Neto
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, FIOCRUZ, Rio de Janeiro, RJ, Brazil FIOCRUZ da Mata Atlântica, FIOCRUZ, Brazil
R.V. Vilela
Affiliation:
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, FIOCRUZ, Rio de Janeiro, RJ, Brazil
*
Author for correspondence: R.O. Simões, E-mail: [email protected]
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Abstract

Nematodes of the genus Physaloptera are globally distributed and more than 100 species are known. Their life cycle involves insects, including beetles, cockroaches and crickets, as intermediate hosts. This study describes a new species of Physaloptera and reports molecular phylogenetic analyses to determine its relationships within the family Physalopteridae. Physaloptera amazonica n. sp. is described from the stomach of the caviomorph rodent Proechimys gardneri collected in the Amazon rainforest in the state of Acre, Brazil. The species is characterized by the male having the first and second pair of sessile papillae asymmetrically placed, lacking a median papilla-like protuberance between the third pairs of sessile papillae, differentiated by size and shape of the spicules, while females have four uterine branches. For both nuclear 18S rRNA and MT-CO1 gene-based phylogenies, we recovered Turgida sequences forming a clade nested within Physaloptera, thus making Physaloptera paraphyletic to the exclusion of Turgida, suggesting that the latter may have evolved from the former monodelphic ancestral state to a derived polydelphic state, or that some species of Physaloptera may belong to different genera. Relationships between most taxa within Physaloptera were poorly resolved in our phylogenies, producing multifurcations or a star phylogeny. The star-like pattern may be attributed to evolutionary processes where past simultaneous species diversification events took place. Physaloptera amazonica n. sp. formed an independent lineage, separately from the other species of Physaloptera, thus supporting the status of a new species. However, all molecular data suggested a closer relationship with other Neotropical species. In conclusion, we added a new species to this already largely diverse genus Physaloptera, bringing new insights to its phylogenetic relationships. Further analyses, adding more species and markers, should provide a better understanding of the evolutionary history of physalopterids.

Keywords

Brazilnematoderodent
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e68
Copyright
Copyright © Cambridge University Press 2019 

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References

Abascal, F, Zardoya, R and Telford, MJ (2010) TranslatorX: Multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Research 38, w7–13.Google Scholar
Almeida, FC, Giannini, NP, DeSalle, R and Simmons, NB (2011) Evolutionary relationships of the old world fruit bats (Chiroptera, Pteropodidae): Another star phylogeny? BMC Evolutionary Biology 11, 281.Google Scholar
Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the nematode parasites of vertebrates. Archival volume. 463 pp. Wallingford, UK, CABI Publishing.Google Scholar
Castillo, AH, Cortinas, MN and Lessa, EP (2005) Rapid diversification of South American Tuco-Tucos (Ctenomys; Rodentia, Ctenomyidae): Contrasting mitochondrial and nuclear intron sequences. Journal of Mammalogy 86, 170–179.Google Scholar
Chabaud, AG (1975) Keys to genera of the Order Spirurida. pp. 1–27 in Anderson, RC, Chabaud, AG, Wilmont, S (Eds) CHI keys to the nematode parasites of vertebrates. United Kingdom, Commonweal.Google Scholar
Ederli, NB, Gallo, SSM, Oliveira, LC and de Oliveira, FCR (2018) Description of a new species Physaloptera goytaca n. sp. (Nematoda, Physalopteridae) from Cerradomys goytaca Tavares, Pessôa & Gonçalves, 2011 (Rodentia, Cricetidae) from Brazil. Parasitology Research 117, 2757–2766.Google Scholar
Edgard, RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Eler, ES, Da Silva, MNF, Silva, CEF and Feldberg, E (2012) Comparative cytogenetics of spiny rats of the genus Proechimys (Rodentia, Echimyidae) from the Amazon region. Genetics and Molecular Research 11, 830–846.Google Scholar
Emmons, LH and Feer, F (1997) Neotropical rainforest mammals. A field guide. 2nd edn. 396 pp. Chicago, University of Chicago Press.Google Scholar
Faith, DP and Cranston, PS (1991) Could a cladogram this short have arisen by chance alone?: On permutation tests for cladistic structure. Cladistics 7, 1–28.Google Scholar
Galewski, T, Mauvrey, JF, Leite, YLR, Patton, JL and Douzery, EJP (2005) Ecomorphological diversification among South American spiny rats (Rodentia; Echimyidae): a phylogenetic and chronological approach. Molecular Phylogenetics Evolution 34, 601–615.Google Scholar
Gannon, WL and Sikes, RS (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy 92, 235–253.Google Scholar
Goldberg, SR and Bursey, CR (2002) Gastrointestinal helminths of seven gekkonid lizard species (Sauria: Gekkonidae) from Oceania. Journal of Natural History 36, 2249–2264.Google Scholar
Hobmaier, M (1941) Extramammalian phase of Physaloptera maxillaris Molin, 1860 (Nematoda). Journal of Parasitology 27, 233.Google Scholar
Honisch, M and Krone, O (2008) Phylogenetic relationships of Spiruromorpha from birds of prey based on 18S rDNA. Journal of Helminthology 82, 129–33.Google Scholar
Humberg, RMP, Tavares, LER, Paiva, F, Oshiro, ET, Bonamigo, RA, Júnior, NT and Oliveira, AG (2011) Turgida turgida (Nematoda: Physalopteridae) parasitic in white-bellied opossum, Didelphis albiventris (Marsupialia: Didelphidae), state of Mato Grosso do Sul, Brazil. Pesquisa Veterinária Brasileira 31, 78–80.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, Meintjes, 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
Kolaczkowski, B and Thornton, JW (2004) Performance of maximum parsimony and likelihood phylogenetics when evolution is heterogeneous. Nature 431, 980–984.Google Scholar
Leite, YLR and Patton, JL (2002) Evolution of South American spiny rats (Rodentia, Echimyidae): The star-phylogeny hypothesis revisited. Molecular Phylogenetics and Evolution 25, 455–464.Google Scholar
Maddison, WP and Maddison, DR (2018), Mesquite: A modular system for evolutionary analysis. Version 1.0. http://www.mesquiteproject.org.Google Scholar
Migueis, R (2001) Uma introdução à geografia do Amazonas. 132 pp. Boa Vista, Gráfica Real.Google Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In 2010 Gateway Computing Environments Workshop, (GCE), 14 November 2010. New Orleans, Louisiana, pp. 1–8.Google Scholar
Morgan, BB (1947) Host-parasite relationships and geographical distribution of the Physaloptera (Nematode). Transaction Wisconsin Academy Sciences, Arts and Letters Illinois 38, 273–292.Google Scholar
Nilsson, RH, Ryberg, M, Kristiansson, E, Abarenkov, K, Larsson, KH and Kõljalg, U (2006) Taxonomic reliability of DNA sequences in public sequence databases: A fungal perspective. PLoS One 1, e59.Google Scholar
Ortlepp, RJ (1922) The nematode genus Physaloptera Rudolphi, 1819. Proceedings of the Zoological Society of London 92, 999–1107.Google Scholar
Panti-May, JA, Hernández-Betancourt, SF, Rodríguez-Vivas, RI and Robles, MR (2015) Infection levels of intestinal helminths in two commensal rodent species from rural households in Yucatan, Mexico. Journal of Helminthology 89, 42–48.Google Scholar
Patton, J and Leite, Y (2015) Genus Proechimys J.A. Allen, 1899. pp. 950–988 in Patton, JL, Pardiñas, UF, D’Elía, G (Eds) Mammals of South America. vol. 2. Rodents. Chicago, University of Chicago Press.Google Scholar
Pereira, FB, Alves, PV, Rocha, BM, Lima, SS and Luque, JL (2012) A new Physaloptera (Nematoda: Physalopteridae) parasite of Tupinambis merianae (Squamata: Teiidae) from southeastern Brazil. Journal of Parasitology 98, 1227–1123.Google Scholar
Pereira, FB, Alves, PV, Rocha, BM, Lima, SS and Luque, JL (2014) Physaloptera bainae n. sp. (Nematoda: Physalopteridae) parasitic in Salvator merianae (Squamata: Teiidae), with a key to Physaloptera species parasitizing reptiles from Brazil. Journal of Parasitology 100, 221–227.Google Scholar
Poon, AFY, Walker, LW, Murray, H, McCloskey, RM, Harrigan, PR and Liang, RH (2013) Mapping the shapes of phylogenetic trees from human and zoonotic RNA viruses. PLoS One 8, e78122.Google Scholar
Portal Amazônia (2016) Amazônia de A a Z. Epi Info. Available at http://www.portalamazonia.com.br/secao/amazoniadeaz/interna.php?id=134 (accessed 10 November 2018).Google Scholar
Price, MN, Dehal, PS and Arkin, AP (2010) FastTree 2 – Approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490.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
Pruesse, E, Peplies, J and Glöckner, FO (2012) SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823–1829.Google Scholar
Quadros, RM, Marques, SMT, Moura, AB and Antonelli, M (2014) First report of the nematode Physaloptera praeputialis parasitizing a jaguarandi. Neotropical Biology and Conservation 9, 186–189.Google Scholar
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.Google Scholar
Ronquist, F, Teslenko, M, Mark, PVD, 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, 539–542.Google Scholar
Russo, CAM, Takezaki, N and Nei, M (1996) Efficiencies of different genes and different tree-building methods in recovering a known vertebrate phylogeny. Molecular Biology and Evolution 13, 525–536.Google Scholar
São Luiz, J, Simões, RO, Torres, EL, Barbosa, HS, Santos, JN, Giese, EG, Rocha, FL and Maldonado, A Jr (2015) A new species of Physaloptera (Nematoda: Physalopteridae) from Cerradomys subflavus (Rodentia: Sigmodontinae) in the Cerrado Biome, Brazil. Neotropical Helminthology 9, 301–312.Google Scholar
Silva, JMC, Rylands, AB and Fonseca, GAB (2005) The fate of the Amazonian areas of endemism. Conservation Biology 19, 688–694.Google Scholar
Sokal, RR and Rohlf, FJ (1995) Biometry: the principles and practice of statistics in biological research. New York, W.H Freeman, p. 886.Google Scholar
Swofford, DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland, MA, Sinauer Associates.Google Scholar
Travassos, L (1920) Contribuições para o conhecimento da fauna helmintológica brasileira. X. Sobre as espécies do gênero Turgida. Memórias do Instituto Oswaldo Cruz 12, 73–77.Google Scholar
Vicente, JJ, Rodrigues, HO, Gomes, DC and Pinto, RM (1997) Nematóides do Brasil. Parte V: Nematóides de mamíferos. Revista Brasileira de Zoologia 14, 1–452.Google Scholar
Vilgalys, R (2003) Taxonomic misidentification in public DNA databases. New Phytologist 160, 4–5.Google Scholar
Warnow, T (2012) Standard maximum likelihood analyses of alignments with gaps can be statistically inconsistent. PLOS Currents 4, 1–14.Google Scholar
Xia, X (2018) DAMBE7: New and improved tools for data analysis in molecular biology and evolution. Molecular Phylogenetics and Evolution 35, 1550–1552.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 phylogenetic analysis and hypothesis testing. Cambridge, Cambridge University Press.Google Scholar
Xia, X, Xie, Z, Salemi, M, Chen, L and Wang, M (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1–7.Google Scholar
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