Molecular phylogenetic position of Haplometroides intercaecalis (Digenea, Plagiorchiidae)

Maria Isabel Müller; Drausio Honorio Morais; Reinaldo José da Silva

doi:10.1515/ap-2018-0062

Article

Molecular phylogenetic position of Haplometroides intercaecalis (Digenea, Plagiorchiidae)

Maria Isabel Müller , Drausio Honorio Morais and Reinaldo José da Silva

Published/Copyright: July 4, 2018

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From the journal Acta Parasitologica Volume 63 Issue 3

Abstract

Three valid species of Haplometroides Odhner, 1910 parasitise snakes and amphisbaenians from South America. This study provides additional data on morphometric and molecular phylogenetic position inferred from the nuclear ribosomal gene 28S (partial). DNA sequences were isolated from Haplometroides intercaecalisSilva, Ferreira and Strüssmann, 2007 found in one specimen of Phalotris matogrossensisLema, D’Agostini and Cappellari, 2005. Five digenean specimens were recovered from the esophagus of this snake, and four specimens were used for morphometrical studies and one specimen for molecular analysis. Phylogenetic analysis using maximum likelihood and Bayesian methods was conducted with sequences available for the order Plagiorchiida and its phylogenetic position places H. intercaecalis among the brachycoeliids Brachycoelium (Dujardin, 1845) Stiles and Hassall, 1898 and Parabrachycoelium Pérez-Ponce de León, Mendoza-Garfias, Razo-Mendivil and Parra-Olea, 2011, and the mesocoeliid Mesocoelium Odhner, 1910, not closely related to plagiorchids as expected. Due to morphological differences among these families, it may be necessary to create a new family to accommodate Haplometroides spp. However, more genera/taxa as well as other molecular markers should be added in future studies to confirm our results and resolve this matter. This is the first phylogenetic positioning of digeneans of the genus Haplometroides, contributing to the systematic analysis of the helminthological biodiversity of Neotropical snakes.

Keywords: Phalotris matogrossensis; 28S rDNA gene; parasite; neotropical snakes

Acknowledgments

We would like to acknowledge colleagues from the laboratory who helped us with fieldwork and Companhia Energética de São Paulo (CESP) for logistical support and authorization to work in RPPN Foz do Rio Aguapeí. We also thank the anonymous reviewers for their valuable help improving the manuscript. Financial support for this study was provided by Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). M.I.M. is supported by CAPES (grant number AUX-PE-PNPD 3005/2010) and the Young Researcher Program (PROPE-UNESP 02/2016). D.H.M is supported by CAPES/PNPD #22005013001P4. R.J.S. is supported by CNPq (309125/2017-0), CNPq-PROTAX (440496/2015-2), and FAPESP 2016/50377-1.

References

Brooks D.R., O’Grady R.T., Glen D.R. 1985. Phylogenetic analysis of the Digenea (Platyhelminthes: Cercomeria) with comments on their adaptive radiation. Canadian Journal of Zoology, 63, 411–443. 10.1139/z85-062Search in Google Scholar

Brooks D.R., Bandoni S.M., MacDonald C.M., O’Grady R.T. 1989. Aspects of the phylogeny of the Trematoda Rudolphi, 1808 (Platyhelminthes: Cercomeria). Canadian Journal of Zoology, 67, 2609–2624. 10.1139/z89-370Search in Google Scholar

Edgar R.C. 2004. Muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5,113. 10.1186/1471-2105-5-113Search in Google Scholar PubMed PubMed Central

Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hosdijk W., Gascuel O. 2010. New algorithms and methods to estimate Maximum-Likelihood Phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321. 10.1093/sysbio/syq010Search in Google Scholar PubMed

Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., et al. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. 10.1093/bioinformatics/bts199Search in Google Scholar PubMed PubMed Central

Kimura M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–12010.1007/BF01731581Search in Google Scholar PubMed

Lema T., DÁgostini M.F., Cappellari L.H. 2005. Nova espécie de Phalotris, redescrição de P. tricolor e osteologia craniana (Serpentes, Elapomorphinae). Iheringia, 95, 65–7810.1590/S0073-47212005000100010Search in Google Scholar

Maldonado J.A., Loker E.S., Morgan J.A.T., Rey L., Lanfredi R.M. 2001. Description of the adult worms of a new Brazilian isolate of Echinostoma paraensis (Platyhelminthes: Digenea) from its natural vertebrate host Nectomys squamipes by light and scanning electron microscopy and molecular analysis. Parasitology Research, 87, 840–84810.1007/s004360100451Search in Google Scholar PubMed

Mendoza-Palmero C.A., Blasco-Costa I., Scholz T. 2015. Molecular phylogeny of Neotropical monogeneans (Platyhelminthes: Monogenea) from catfishes (Siluriformes). Parasites and Vectors, 8, 164. 10.1186/s13071-015-0767-8Search in Google Scholar PubMed PubMed Central

Pérez-Ponce de León G., Mendoza-Garfias B., Razo-Mendivil U., Parra-Olea G. 2011. A new genus and species of Brachycoeliidae (Digenea) from Chiropterontriton sp. (Caudata: Plethodontidae) in Mexico and its phylogenetic position within the Plagiorchiida based on partial sequences of the 28S ribosomal RNA gene. Journal of Parasitology, 97, 128–134. 10.1645/GE-2346.1Search in Google Scholar PubMed

Posada D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256. 10.1093/molbev/msn083Search in Google Scholar

Rambaut A. 2009. Molecular evolution, phylogenetics and epidemiology: Fig-Tree. Available at http//tree.bio.ed.ac.uk/software/figtree/ (accessed 10 November 2015)Search in Google Scholar

Razo-Mendivil, U., Pérez-Ponce de Léon, G. 2011. Testing the evolutionary and biogeographical history of Glyphtelmins (Digenea: Plagiorchiida) a parasite of anurans, through a simultaneous analysis of molecular and morphological data. Molecular Phylogenetics and Evolution, 59, 331–341. 10.1016/j.ympev.2011.02.018Search in Google Scholar

Ronquist F., Huelsenbeck J. P. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–157410.1093/bioinformatics/btg180Search in Google Scholar

Santos K.R., Barrella T.H., Zica E.O.P., Silva R.J. 2008. New report on parasitism by Haplometroides buccicola (Digenea, Plagiorchiidae) in brazilian snakes. Journal of Venomous Animals Toxins including Tropical Diseases, 14, 527–53210.1590/S1678-91992008000300011Search in Google Scholar

Silva R.J., Barrella T.H. 2002. Micrurus frontalis as a new host recorded for Haplometroides odhneri (Trematoda, Digenea, Plagiorchiidae). Revista Brasileira de Parasitologia Veterinaria, 11, 47–8Search in Google Scholar

Silva R.J., Andrade P.A., Monteiro e Silva H.A., Rossellini M., Barrella T.H. 2005a. Report on the occurrence of Haplometroides buccicola (Trematoda, Digenea, Plagiorchiidae) infecting Phalotris lativittatus (Serpentes, Colubridae) in Brazil. Journal of Venomous Animals Toxins including Tropical Diseases, 11, 373–910.1590/S1678-91992005000300013Search in Google Scholar

Silva R.J., Zica E.O.P., Cruz M., O’Reilly J.C., Costa M.C. 2005b. Occurrence of Haplometroides odhneri (Trematoda, Digenea, Plagiorchiidae) infecting Leptotyphlops koppesi (Serpentes, Leptotyphlopidae). Arquivos Brasileiros de Medicina Veterinaria e Zootecnia, 57, 267–26910.1590/S0102-09352005000800021Search in Google Scholar

Silva R.J., Ferreira V.L., Strüssmann C. 2007. New species of Haplometroides (Digenea, Plagiorchiidae) from Phalotris nasutus (Gomes, 1915) (Serpentes, Colubridae). Journal of Parasitology, 93, 917–92110.1645/GE-1123R.1Search in Google Scholar

Silva R.J., Béda A.F., Ferreira V.L. 2008. New record of Haplometroides intercaecalis (Digenea, Plagiorchiidae) infecting a Brazilian snake. Journal of Venomous Animals Toxins including Tropical Diseases, 14, 161–16510.1590/S1678-91992008000100013Search in Google Scholar

Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 12, 2725–272910.1093/molbev/mst197Search in Google Scholar

Tkach V., Pawlowski J., Mariaux J. 2000. Phylogenetic analysis of the suborder plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. International Journal for Parasitology, 30, 83–9310.1016/S0020-7519(99)00163-0Search in Google Scholar

Tkach V.V., Grabda-Kazuska B., Swiderski Z. 2001. Systematic position and phylogenetic relationships of the family Omphalometridae (Digenea, Plagiorchiida) inferred from partial lsrDNA sequences. International Journal for Parasitology, 31, 81–8510.1016/S0020-7519(00)00154-5Search in Google Scholar

Tkach V.V. 2008. Family Plagiorchiidae Lühe, 1901. In: (Eds: R.A. Bray, D. Gibson, A. Jones). Keys to the Trematoda. CAB International, Wallingford, Oxfordshire, U.K. Vol. 3, pp. 82410.1079/9780851995885.0295Search in Google Scholar

Vidal V., Ortiz J., Diaz J.I., Zafrilla B., Bonete M.J., Ruiz de Ybañez M.R. et al. 2015. Morphological, molecular and phylogenetic analyses of the spirurid nematode Stegophorus macronectes (Johnston & Mawson,1942). Journal of Helminthology, 1–9. 10.1017/S0022149X15000218Search in Google Scholar PubMed

Xia X. 2013. DAMBE 5. A comprehensive software package for data analysis in molecular biology and evolution. Molecular Biology and Evolution, 30, 1720-1728. 10.1093/molbev/mst064Search in Google Scholar PubMed PubMed Central

Received: 2018-03-05

Revised: 2018-04-10

Accepted: 2018-04-12

Published Online: 2018-07-04

Published in Print: 2018-09-25

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https://doi.org/10.1515/ap-2018-0062

Keywords for this article

Phalotris matogrossensis; 28S rDNA gene; parasite; neotropical snakes