Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-20T00:20:21.482Z Has data issue: false hasContentIssue false

Diaphanocephalus galeatus (Nematoda: Diaphanocephalidae), a poorly known parasite of lizards: redescription, first genetic characterization and a revision of its congeners from Brazil

Published online by Cambridge University Press:  16 July 2018

F.B. Pereira*
Affiliation:
Programa de Pós-Graduação em Biologia Animal, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Av. Costa e Silva s/n°, CEP 79070-900, Campo Grande, MS, Brazil
V.L. Ferreira
Affiliation:
Programa de Pós-Graduação em Biologia Animal, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Av. Costa e Silva s/n°, CEP 79070-900, Campo Grande, MS, Brazil
W.M. Tomas
Affiliation:
Embrapa Pantanal, Rua 21 de Setembro 1880, Nossa Senhora de Fátima, CEP 79320-900, Corumbá, MS, Brazil
C. Elisei
Affiliation:
Programa de Pós-Graduação em Biotecnologia, Universidade Católica Dom Bosco, Av. Tamandaré 6000, Jardim Seminário, Campo Grande, MS, Brazil
F. Paiva
Affiliation:
Programa de Pós-Graduação em Biologia Animal, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Av. Costa e Silva s/n°, CEP 79070-900, Campo Grande, MS, Brazil
L.E.R. Tavares
Affiliation:
Programa de Pós-Graduação em Biologia Animal, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Av. Costa e Silva s/n°, CEP 79070-900, Campo Grande, MS, Brazil
*
Author for correspondence: F.B. Pereira E-mail: [email protected]

Abstract

Diaphanocephalus galeatus collected from the small intestine of the lizard Dracaena paraguayensis in the Pantanal wetlands, State of Mato Grosso do Sul, Brazil, is redescribed. Genetic characterization and observations using scanning electron microscopy (SEM) were performed for the first time. The vouchers of D. galeatus and the type specimens of its congeners, deposited in the Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC), were consulted. Light and SEM observations revealed several undescribed features of D. galeatus, i.e. structure of the cephalic end and of the buccal capsule, position and morphology of deirids, presence of phasmids in females and presence of unpaired papilla on the membranous projection that covers the genital cone in males. After observation of the specimens deposited in the helminthological collection, D. jacuruxi is considered a synonym of D. galeatus, and D. diesingi, despite its incomplete description, is tentatively retained as valid due to the poor condition of the type material. The results also indicated low host specificity of D. galeatus, contradicting previous assertions. Genetic comparisons using patristic distances and phylogenetic trees generated from sequences of the 28S rRNA nuclear gene indicated that D. galeatus is closer to the taxa within Ancylostomatoidea and Strongyloidea than any lineage of Metastrongyloidea or Trichostrongyloidea. However, most of the nodal supports were low. Based on the genetic and morphological characterization, the validity of D. galeatus was confirmed. These data may serve for further comparative approaches for different populations of the parasite, from different hosts in different geographical areas, mitigating taxonomic confusions.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2018 

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

Alho, CJR (1965) Sôbre uma nova espécie do gênero Diaphanocephalus Diesing, 1851, parasita de lagarto da Amazônia (Dracaena guianensis Daudin) (Nematoda, Strongyloidea). Boletim do Museu Paraense Emílio Goeldi 59, 19.Google Scholar
Anderson, RC (2000) Nematode Parasites of Vertebrates: Their Development and Transmission. Wallingford: CABI Publishing.Google Scholar
Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the Nematode Parasites of Vertebrates: Archival Volume. Wallingford: CABI Publishing.Google Scholar
Astrin, JJ, Zhoun, X and Misof, B (2013) The importance of biobanking in molecular taxonomy, with proposed definitions for vouchers in a molecular context. Zookeys 365, 6770.Google Scholar
Ávila, RW and Silva, RJ (2010) Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. The Journal of Venomous Animals and Toxins Including Tropical Diseases 16, 543572.Google Scholar
Baker, MR (1987) Synopsis of the Nematoda parasitic in amphibians and reptiles. Memorial University of Newfoundland, Occasional Papers in Biology 11, 1325.Google Scholar
Blaxter, ML and Koutsovoulos, G (2014) The evolution of parasitism in Nematoda. Parasitology 142, S26S39.Google Scholar
Blaxter, ML et al. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 329, 7175.Google Scholar
Chabaud, AG et al. (1970) Remarques sur l'homologie entre les papilles cloacales des Rhabditides et les côtes dorsales des Strongylida. Comptes Rendus Hebdiomadaire des Séances l'Académie des Sciences 271, 17711774.Google Scholar
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, 16251637.Google Scholar
Chilton, NB et al. (2006) The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Molecular Phylogenetics and Evolution 40, 118128.Google Scholar
Darriba, D et al. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.Google Scholar
Diesing, KM (1851) Systema Helmintum. Vol. 2. Vienna: W. Braumüller.Google Scholar
Durette-Desset, M-C and Chabaud, AG (1993) Nomenclature des Strongylida au-dessus du groupe famille. Annales de Parasitologie Humaine et Comparée 68, 111112.Google Scholar
Durette-Desset, M-C, Beveridge, I and Spratt, DM (1994) The origins and evolutionary expansion of the Strongylida (Nematoda). International Journal for Parasitology 24, 11391165.Google Scholar
Fourment, M and Gibbs, MJ (2006) PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evolutionary Biology 6, 1.Google Scholar
Freitas, JFT and Lent, H (1938) Pesquisas helmintológicas realisadas no estado do Pará. V. Genero Diaphanocephalus Diesing, 1851 (Nematoda: Strongyloidea). Memórias do Instituto Oswaldo Cruz 33, 423432.Google Scholar
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.Google Scholar
Harvey, MB, Ugueto, GN and Gutberlet, RL Jr (2012) Review of teiid morphology with a revised taxonomy and phylogeny of the Teiidae (Lepidosauria: Squamata). Zootaxa 3459, 1156.Google Scholar
Hodda, M (2011) Phylum Nematoda Cobbold, 1932. In Zhang, ZQ (ed.), Animal Biodiversity: An Outline of Higher-Level Classification and Survey of Taxonomic Richness. Auckland, Magnolia Press, pp. 6395.Google Scholar
Huelsenbeck, JP and Ronquist, F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.Google Scholar
Kuzmin, Y et al. (2013) New species of Kalicephalus (Nemadota: Diaphanocephalidae) from a snake, Oxyrhabdium leporinum, on Luzon Island, Philippines. Comparative Parasitology 80, 240246.Google Scholar
Lichtenfels, R (1980) Keys to the genera of Strongylida 4. Diaphanocephaloidea and Ancylostomatoidea. In Anderson, RC, Chabaud, AG and Willmott, S (eds), CIH Keys to the Nematode Parasites of Vertebrates. Farnham Royal, Commonwealth Agricultural Bureaux, pp. 4468.Google Scholar
Medal, BHM et al. (2007) An improved molecular phylogeny of the Nematoda with special emphasis on marine taxa. Molecular Phylogenetics and Evolution 42, 622636.Google 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, 205217.Google Scholar
Nunn, GB (1992) Nematode Molecular Evolution (PhD dissertation). University of Nottingham, UK.Google Scholar
Ortlepp, RJ (1923) Observations on the nematode genera Kalicephalus, Diaphanocephalus, and Occipitodontus g.n., and on the larval development of Kalicephalus philodryadus sp. n. Journal of Helminthology 1, 165189.Google Scholar
Pereira, FB et al. (2015) A morphological and molecular study of two species of Raphidascaroides Yamaguti, 1941 (Nematoda: Anisakidae), parasites of doradid catfish (Siluriformes) in South America, with a description of R. moraveci n. sp. Systematic Parasitology 91, 4961.Google Scholar
Ramalho, ACO et al. (2009) Helminths from an introduced species (Tupinambis merianae), and two endemic species (Trachylepis atlantica and Amphisbaena ridleyi) from Fernando de Noronha Archipelago, Brazil. Journal of Parasitology 95, 10261028.Google Scholar
Rudolphi, CA (1819) Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. Berolini, Augustus Rucker.Google Scholar
Schad, GA (1962) Studies on the genus Kalicephalus (Nematoda: Diaphanocephalidae) II. A taxonomic revision of the genus Kalicephalus Molin, 1861. Canadian Journal of Zoology 40, 10351165.Google Scholar
Teixeira, AAM et al. (2017) Helminths of the lizard Salvator merianae in the Caatinga, northeastern Brazil. Brazilian Journal of Biology 77, 312317.Google Scholar
Uetz, P and Hošek, J (eds) (2018) The Reptile Database. Available at: http//www.reptile-database.org, version 02/2018, accessed 27 March 2017.Google Scholar
Vieira, TD, Fedatto-Bernardon, F and Müller, G (2016) Diaphanocephalus galeatus (Nematoda: Diaphanocephalidae), parasite of Salvator merianae (Squamata: Teiidae) in southern Brazil. Revista Mexicana de Biodiversidad 87, 512515.Google Scholar
Zhang, H, Zhang, S and Zhang, L (2011) Two species of the genus Kalicephalus Molin, 1861 (Nematoda: Diaphanocephaloidea) form the water monitor, Varanus salvator (Laurenti, 1768) in Guangdong Province, China. Acta Parasitologica 56, 4853.Google Scholar
Supplementary material: PDF

Pereira et al. supplementary material

Pereira et al. supplementary material 1

Download Pereira et al. supplementary material(PDF)
PDF 454.2 KB