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The importance of integrative approaches in nematode taxonomy: the validity of Parapharyngodon and Thelandros as distinct genera

Published online by Cambridge University Press:  20 September 2018

A. De Sousa ,
F. Jorge ,
M.A. Carretero ,
D.J. Harris ,
V. Roca  and
A. Perera Open the ORCID record for A. Perera [Opens in a new window]
A. De Sousa
Affiliation:
CIBIO/ InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus de Vairão, 4485-661 Vairão, Portugal
F. Jorge
Affiliation:
Department of Zoology, University of Otago, 340 Great King Street, PO Box 56, Dunedin 9054, New Zealand
M.A. Carretero
Affiliation:
CIBIO/ InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus de Vairão, 4485-661 Vairão, Portugal
D.J. Harris
Affiliation:
CIBIO/ InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus de Vairão, 4485-661 Vairão, Portugal Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua Campo Alegre, 4169-007, Porto, Portugal
V. Roca
Affiliation:
Departament de Zoologia, Facultat de Ciències Biològiques, Universitat de València. Dr. Moliner, 50, 46100 Burjassot, Spain
A. Perera*
Affiliation:
CIBIO/ InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus de Vairão, 4485-661 Vairão, Portugal
*
Author for correspondence: A. Perera, E-mail: perera@cibio.up.pt
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Abstract

Despite the advances of molecular tools, new nematode species are still described mainly based on morphological characters. Parapharyngodon and Thelandros are two genera of oxyurids with unclear related taxonomic histories. Here we use morphological characters (linear measurements and categorical variables) and genetic information (18S rRNA, 28S rRNA and COI partial gene sequences) to confirm the relationships between representatives of these two genera and to determine whether they can be discriminated morphologically. Genetic results confirm the existence of two main clades, mostly congruent with Parapharyngodon and Thelandros genera but with several discordances. Thelandros is polyphyletic, with two of the species analysed (T. filiformis and T. tinerfensis) being part of the Thelandros clade, but with a third one (T. galloti) falling within the Parapharyngodon clade. Regarding the Parapharyngodon clade, P. cubensis, P. scleratus and Parapharyngodon sp. from Mexico form congruent lineages, while most P. echinatus samples cluster in another group, with one exception. Interestingly, P. micipsae samples are scattered across the Parapharyngodon clade, suggesting that they were misidentified or rather represent alternative morphotypes of other species. Morphological analysis identified the length of the tail, number of caudal papillae, position of the nerve ring, presence of caudal alae and length of the lateral alae as reliable characters to distinguish between Parapharyngodon and Thelandros genetic clades. Our study highlights the current taxonomic inconsistency in these groups, mainly derived from the exclusive use of morphological data. As such, we advocate for the routine implementation of molecular data in nematode taxonomic studies.

Type
Research Paper
Information
Journal of Helminthology , Volume 93 , Issue 5 , September 2019 , pp. 616 - 628
Copyright
Copyright © Cambridge University Press 2018 

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References

Adams, DC and Otárola-Castillo, E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology & Evolution 4, 393–399.Google Scholar
Adamson, ML (1981) Parapharyngodon osteopili n. sp. (Pharyngodonidae: Oxyuroidea) and a revision of Parapharyngodon and Thelandros. Systematic Parasitology 3, 105–117.Google Scholar
Adamson, ML and Nasher, AK (1984) Pharyngodonids (Oxyuroidea; Nematoda) of Agama adramitana in Saudi Arabia with notes on Parapharyngodon. Canadian Journal of Zoology 62, 2600–2609.Google Scholar
Ainsworth, R (1990) Male dimorphism in two new species of nematodes (Pharyngodonidae: Oxyurida) from New Zealand lizards. Journal of Parasitology 76, 812–822.Google Scholar
Astasio-Arbiza, P et al. (1988) Thelandros galloti n. sp. (Nematoda, Pharyngodonidae) sobre Gallotia galloti galloti Duméril y Bibron, 1839, lacértido endémico de Tenerife (Islas Canarias). Revista Ibérica de Parasitología 48, 283–288.Google Scholar
Astasio-Arbiza, P et al. (1989) Descripción de Thelandros filiformis n. sp. (Nematoda: Pharyngodonidae) sobre Gallotia galloti galloti Duméril y Bibron, 1839 de la isla de Tenerife (Islas Canarias). Revista Ibérica de Parasitología 49, 45–50.Google Scholar
Baylis, HA (1936) The Fauna of British India, including Ceylon and Burma. Nematoda. Vol. I. Ascaridoidea and Strongyloidea. London: Taylor & Francis.Google Scholar
Borges, JN et al. (2012) Morphological and molecular diagnosis of anisakid nematode larvae from cutlassfish (Trichiurus lepturus) off the coast of Rio de Janeiro, Brazil. PLoS ONE 7, e40447.Google Scholar
Bursey, CR and Goldberg, SR (2005) Two new species of Pharyngodonidae (Nematoda: Oxyuroidea) and other nematodes in Agama caudospina (Squamata: Agamidae) from Kenya, Africa. Journal of Parasitology 91, 591–599.Google Scholar
Bursey, CR and Goldberg, SR (2015) Description of a new species of Parapharyngodon (Nematoda: Pharyngodonidae) from Mexico, with a list of current species and key to the species from the Panamanian Region. Journal of Parasitology 101, 374–381.Google Scholar
Carretero, MA et al. (2006) Diet and helminth parasites in the Gran Canaria giant lizard Gallotia stehlini. Revista Española de Herpetología 20, 105–117.Google Scholar
Castaño-Fernández, C, Zapatero-Ramos, LM and Puertas, S (1987) Revision of genera Parapharyngodon Chatterji, 1933 and Thelandros Wedl, 1862 (Oxyuroidea, Pharyngodonidae). Revista Ibérica de Parasitología 47, 271–274.Google Scholar
Castresana, J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.Google Scholar
Chabaud, AG and Golvan, YJ (1957) Miscellanea helminthologica maroccana XXIV. Nématodes parasites de lézards de la foret de Nefifik. Archives de l'Institut Pasteur de Maroc 7, 447–469.Google Scholar
Chatterji, RC (1933) On a new nematode, Parapharyngodon maplestoni gen. nov., sp. nov., from a Burmese lizard. Annals of Tropical Medicine and Parasitology 27, 131–134.Google Scholar
Chaudhary, A et al. (2015) New molecular data for parasites Hammerschmidtiella indicus and Thelandros scleratus (Nematoda: Oxyurida) to infer phylogenetic position. Turkish Journal of Zoology 39, 251–255.Google Scholar
Chaudhary, A et al. (2017) Molecular identification of Thelandros scleratus and Thelastoma icemi (Nematoda: Oxyurida) using mitochondrial cox 1 sequences. Acta Parasitologica 62, 382–385.Google Scholar
De Ley, P et al. (2005) An integrated approach to fast and informative morphological vouchering of nematodes for applications in molecular barcoding. Philosophical Transactions of the Royal Society of London, Series B 272, 1945–1958.Google Scholar
De Sousa, A et al. (2017) First record of Thelandros sp. Wedl, 1862 pinworms (Nematoda: Oxyurida: Pharyngodonidae) on São Vicente Island, Cabo Verde. Zoologia Caboverdiana 6, 15–18.Google Scholar
Derycke, S et al. (2010) Linking DNA sequences to morphology: cryptic diversity and population genetic structure in the marine nematode Thoracostoma trachygaster (Nematoda, Leptosomatidae). Zoologica Scripta 39, 276–289.Google Scholar
Dobson, A et al. (2008) Homage to Linnaeus: how many parasites? How many hosts? Proceedings of the National Academy of Sciences of the USA 105, S11482–S11489.Google Scholar
Dorris, M, De Ley, P and Blaxter, ML (1999) Molecular analysis of nematode diversity and the evolution of parasitism. Parasitology Today 15, 188–193.Google Scholar
Dung, BT, Bursey, C and Goldberg, SR (2009) A new species of Thelandros (Nematoda, Oxyuroidea, Pharyngodonidae) in Leiolepis reevesi (Sauria, Agamidae) from Vietnam. Acta Parasitologica 54, 151–153.Google Scholar
Falk, BG and Perkins, SL (2013) Host specificity shapes population structure of pinworm parasites in Caribbean reptiles. Molecular Ecology 22, 4576–4590.Google Scholar
Floyd, RM et al. (2005) Nematode-specific PCR primers for the 18S small subunit rRNA gene. Molecular Ecology Notes 5, 611–612.Google Scholar
Garduño-Montes de Oca, EU, Mata-López, R and León-Règagnon, V (2016) Two new species of Parapharyngodon parasites of Sceloporus pyrocephalus, with a key to the species found in Mexico (Nematoda, Pharyngodonidae). Zookeys 559, 1–16.Google Scholar
Gelman, A and Rubin, DB (1992) Inference from iterative simulation using multiple sequences. Statistical Science 7, 457–511.Google Scholar
Goswami, U et al. (2016) Molecular and ultrastructure characterization of two nematodes (Thelandros scleratus and Physalopteroides dactyluris) based on ribosomal and mitochondrial DNA sequences. Helminthologia 53, 165–171.Google Scholar
Harrell, FE Jr et al. (2017) Hmisc: Harrell Miscellaneous. R package version 4.0-3. https://CRAN.R-project.org/package=HmiscGoogle Scholar
Hassan, EA (2016) Nematode community infecting Chalcides ocellatus lizard and their relation to some environmental and biological factors. Journal of the Egyptian Society of Parasitology 46, 399–406.Google Scholar
Hering-Hagenbeck, SFBN, Petter, AJ and Boomker, J (2002) Redescription of some Spauligodon spp. and Parapharyngodon spp., and of Skrjabinodon mabuyae (Sandground, 1936) Inglis, 1968 (Pharyngodonidae: Oxyuroidea) from insectivorous South African lizards. Onderstepoort Journal of Veterinary Research 68, 7–29.Google Scholar
Jorge, F et al. (2011) A phylogenetic assessment of the colonisation patterns in Spauligodon atlanticus Astasio-Arbiza et al., 1987 (Nematoda: Oxyurida: Pharyngodonidae), a parasite of lizards of the genus Gallotia Boulenger: no simple answers. Systematic Parasitology 80, 53–66.Google Scholar
Jorge, F et al. (2013) Cryptic species unveiled: the case of the nematode Spauligodon atlanticus. Journal of Zoological Systematics and Evolutionary Research 51, 187–202.Google Scholar
Jorge, F et al. (2014) Evolution of alternative male morphotypes in oxyurid nematodes: a case of convergence? Journal of Evolutionary Biology 27, 1631–1643.Google Scholar
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.Google Scholar
Katoh, K, Rozewicki, J and Yamada, KD (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, bbx108. doi: 10.1093/bib/bbx108Google Scholar
Katoh, K et al. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.Google Scholar
Kearse, M et al. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.Google Scholar
Lanfear, R et al. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.Google Scholar
Martin, JE and Roca, V (2004) Helminth infracommunities of Gallotia caesaris caesaris and Gallotia caesaris gomerae (Sauria: Lacertidae) from the Canary Islands (Eastern Atlantic). Journal of Parasitology 90, 266–270.Google Scholar
Martin, JE and Roca, V (2005) Helminths of the Atlantic lizard, Gallotia atlantica (Reptilia: Lacertidae), in the Canary Islands (Eastern Atlantic): composition and structure of component communities. Acta Parasitologica 50, 85–89.Google Scholar
Mašová, Š et al. (2008) Morphometric and molecular characterization of Parapharyngodon echinatus (Nematoda, Pharyngodonidae) from the Senegal gecko (Tarentola parvicarinata). Acta Parasitologica 53, 274–283.Google Scholar
Mašová, Š et al. (2009) Redescription of Parapharyngodon micipsae (Seurat 1917) (Nematoda Pharyngodonidae) from the new host Tarentola parvicarinata Joger 1980 (Squamata Gekkonidae). Tropical Zoology 22, 243–255.Google Scholar
Moravec, F, Barus, V and Rysavy, B (1987) On parasitic nematodes of the families Heterakidae and Pharyngodonidae from reptiles in Egypt. Folia Parasitologica 34, 269–280.Google Scholar
Nadler, SA and Pérez-Ponce de León, G (2011) Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138, 1688–1709.Google Scholar
Ott, JA, Leisch, N and Gruber-Vodicka, HR (2014) Eubostrichus fertilis sp. n., a new marine nematode (Desmodoridae: Stilbonematinae) with an extraordinary reproductive potential from Belize, Central America. Nematology 16, 777–787.Google Scholar
Paradis, E, Claude, J and Strimmer, K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290.Google Scholar
Pereira, FB et al. (2017) Parapharyngodon hugoi n. sp., a new nematode (Oxyuroidea: Pharyngodonidae) of the tree frog Trachycephalus typhonius (Linnaeus) from the Brazilian Pantanal, including a key to the congeners from amphibians of the American continent. Systematic Parasitology 94, 599–607.Google Scholar
Petter, AJ and Quentin, JC (2009) Oxyurida: Oxyuroidea. In Anderson, RC, Chabaud, AG and Willmott, S (eds), Keys to the Nematode Parasites of Vertebrates: Archival Volume. London: CAB International, pp. 218–247.Google Scholar
Prosser, SW et al. (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
R Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rambaut, A (2014) FigTree. Version 1.4.2. University of Edinburgh, Edinburgh, UK. Available at: Tree.bio.ed.ac.uk/software/figtree/.Google Scholar
Ristau, K, Steinfartz, S and Traunspurger, W (2013) First evidence of cryptic species diversity and significant population structure in a widespread freshwater nematode morphospecies (Tobrilus gracilis). Molecular Ecology 22, 4562–4575.Google Scholar
Rizvi, AN, Maiti, P and Bursey, CR (2017) Three new species of Pharyngodonidae (Nematoda: Oxyuridea) in Laudakia tuberculata (Squamata: Agamidae) from Dehradun, Uttarakhand, India. Acta Parasitologica 62, 273–289.Google Scholar
Roca, V (1985) Contribución al conocimiento de la helmintofauna de los lacértidos y gekónidos del piso termomediterráneo del levante ibérico (PhD thesis). Facultad de Ciencias Biológicas, Universidad de Valencia. Valencia.Google Scholar
Roca, V et al. (2005) Helminth communities of two lizard populations (Lacertidae) from Canary Islands (Spain): host diet–parasite relationships. Amphibia-Reptilia 26, 535–542.Google Scholar
Ronquist, F et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
RStudio Team (2015) RStudio: Integrated Development for R. RStudio, Inc., Boston, MA, USA. Available at http://www.rstudio.com/.Google Scholar
Ruiz Sanchez, SL (1996) Estudio de nematodos parásitos de lacértidos de la provincia de Tenerife (PhD thesis). Universidad Complutense de Madrid, Madrid, Spain.Google Scholar
Seurat, LG (1917) Sur les Oxyures des Sauriens du Nord-Africain. Archives de Zoologie Expérimentale et Générale 56, 401–404.Google Scholar
Solera-Puertas, MA et al. (1988) Descripción de Thelandros tinerfensis n. sp. (Nematoda, Pharyngodonidae) sobre Chalcides viridanus Boulenger, 1887 y Gallotia galloti galloti Duméril y Bibron, 1839, de la isla de Tenerife (Islas Canarias). Revista Ibérica de Parasitología 48, 33–39.Google Scholar
Talavera, G and Castresana, J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.Google Scholar
Tamura, K et al. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Teixeira de Freitas, JF (1957) Sôbre os gêneros Thelandros Wedl, 1862 e Parapharyngodon Chatterji, 1933, com descrição de Parapharyngodon alvarengai sp. n. (Nematoda, Oxyuroidea). Memórias do Instituto Oswaldo Cruz 55, 21–45.Google Scholar
Whiting, MF (2002) Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31, 93–104.Google Scholar
Yamaguti, S (1961) Systema Helminthum. Vol. 3. The Nematodes of Vertebrates. New York, NY: Wiley Interscience.Google Scholar
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