Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-26T08:14:22.678Z Has data issue: false hasContentIssue false
  • English
  • Français

Remarkable morphological variation in the proboscis of Neorhadinorhynchus nudus (Harada, 1938) (Acanthocephala: Echinorhynchida)

Published online by Cambridge University Press:  27 September 2018

Liang Li Open the ORCID record for Liang Li [Opens in a new window] ,
Matthew Thomas Wayland ,
Hui-Xia Chen  and
Yue Yang
Liang Li*
Affiliation:
Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei Province, College of Life Sciences, Hebei Normal University, 050024 Shijiazhuang, Hebei Province, P. R. China
Matthew Thomas Wayland
Affiliation:
Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, UK
Hui-Xia Chen
Affiliation:
Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei Province, College of Life Sciences, Hebei Normal University, 050024 Shijiazhuang, Hebei Province, P. R. China
Yue Yang
Affiliation:
Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei Province, College of Life Sciences, Hebei Normal University, 050024 Shijiazhuang, Hebei Province, P. R. China
*
Author for correspondence: Liang Li, E-mail: liangliangex369@126.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The acanthocephalans are characterized by a retractible proboscis, armed with rows of recurved hooks, which serves as the primary organ for attachment of the adult worm to the intestinal wall of the vertebrate definitive host. Whilst there is a considerable variation in the size, shape and armature of the proboscis across the phylum, intraspecific variation is generally regarded to be minimal. Consequently, subtle differences in proboscis morphology are often used to delimit congeneric species. In this study, striking variability in proboscis morphology was observed among individuals of Neorhadinorhynchus nudus (Harada, 1938) collected from the frigate tuna Auxis thazard Lacépède (Perciformes: Scombridae) in the South China Sea. Based on the length of the proboscis, and number of hooks per longitudinal row, these specimens of N. nudus were readily grouped into three distinct morphotypes, which might be considered separate taxa under the morphospecies concept. However, analysis of nuclear and mitochondrial DNA sequences revealed a level of nucleotide divergence typical of an intraspecific comparison. Moreover, the three morphotypes do not represent three separate genetic lineages. The surprising, and previously undocumented level of intraspecific variation in proboscis morphology found in the present study, underscores the need to use molecular markers for delimiting acanthocephalan species.

Keywords

DNA taxonomyfrigate tunamorphological variabilityNeoechinorhynchusphylogenyproboscis armature
Type
Research Article
Information
Parasitology , Volume 146 , Issue 3 , March 2019 , pp. 348 - 355
Check for updates
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

Amin, OM (1975) Variability in Acanthocephalus parksidei Amin, 1974 (Acanthocephala: Echinorhynchidae). Journal of Parasitology 61, 307–317.Google Scholar
Amin, OM (1984) Variability and redescription of Acanthocephalus dirus (Acanthocephala: Echinorhynchidae) from freshwater fishes in North America. Proceedings of the Helminthological Society of Washington 51, 225–237.Google Scholar
Amin, OM (2013) Classification of the Acanthocephala. Folia Parasitologica 60, 273–305.Google Scholar
Amin, OM and Ha, NV (2011) On four species of echinorhynchid acanthocephalans from marine fish in Halong Bay, Vietnam, including the description of three new species, and a key to the species of Gorgorhynchus. Parasitology Research 109, 841–847.Google Scholar
Amin, OM and Nahhas, FM (1994) Acanthocephala of marine fishes off Fiji Islands, with descriptions of Filisoma longcementglandus n. sp., Neorhadinorhynchus macrospinosus n. sp. (Cavisomidae), and gravid females of Rhadinorhynchus johnstoni (Rhadinorhynchidae); and keys to species of the genera Filisoma and Neorhadinorhynchus. Journal of Parasitology 80, 768–774.Google Scholar
Amin, OM and Redlin, MJ (1980) The effect of host species on growth and variability of Echinorhynchus salmonis Müller, 1784 (Acanthocephala: Echinorhynchidae), with special reference to the status of the genus. Systematic Parasitology 2, 9–22.Google Scholar
Amin, OM, Evans, P, Heckmann, RA and El-Naggar, AM (2013) The description of Mediorhynchus africanus n. sp. (Acanthocephala: Gigantorhynchidae) from galliform birds in Africa. Parasitology Research 112, 2897–2906.Google Scholar
Awachie, JBE (1966) The development and life history of Echinorhynchus truttae Schrank, 1788 (Acanthocephala). Journal of Helminthology 40, 11–32.Google Scholar
Braicovich, PE, Lanfranchi, AL, Farber, MD, Marvaldi, AE, Luque, JL and Timi, JT (2014) Genetic and morphological evidence reveals the existence of a new family, genus and species of Echinorhynchida (Acanthocephala). Folia Parasitologica 61, 377–384.Google Scholar
Brown, AF (1987) Anatomical variability and secondary sexual characteristics in Pomphorhynchus laevis (Müller, 1776) (Acanthocephala). Systematic Parasitology 9, 213–219.Google Scholar
Buckner, SC and Nickol, BB (1975) Morphological variation of Moniliformis moniliformis (Bremser, 1811) Travassos, 1915 and Moniliformis clarki (Ward, 1917) Chandler 1921. Journal of Parasitology 61, 996–998.Google Scholar
Buron, Id, Renaud, F and Euzet, L (1986) Speciation and specificity of acanthocephalans. Genetic and morphological studies of Acanthocephaloides geneticus sp. nov. parasitizing Arnoglossus laterna (Bothidae) from the Mediterranean littoral (Sète – France). Parasitology 92, 165–171.Google Scholar
Cain, AJ (1953) Geography, ecology and coexistence in relation to the biological definition of the species. Evolution 7, 76–83.Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.Google Scholar
Fukui, T and Morisita, T (1937) Studies on the Acanthocephala of Japan. Jikken. Igaku Zasshi 21, 36–41 [In Japanese].Google Scholar
García-Varela, M and Nadler, SA (2005) Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. Journal of Parasitology 91, 1401–1409.Google Scholar
Garey, JR, Near, TJ, Nonnemacher, MR and Nadler, SA (1996) Molecular evidence for Acanthocephala as a subtaxon of Rotifera. Journal of Molecular Evolution 43, 287–292.Google Scholar
Golvan, YJ (1969) Systématique des Acanthocéphales (Acanthocephala Rudolphi, 1801), L'ordre des Palaeacanthocephala Meyer, 1931, La superfamille des Echinorhynchidea (Cobbold, 1876) Golvan et Houin 1973. Mémoires du Muséum Nationale d'Histoire Naturelle 47, 1–373.Google Scholar
Goméz, A, Serra, M, Carvalho, GR and Lunt, DH (2002) Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 56, 1431–1444.Google Scholar
Grabda-Kazubska, B and Ejsymont, L (1969) Studies on the morphology, variability and systematic status of Echinorhynchus borealis Linstow, 1901 (Acanthocephala, Echinorhynchidae). Acta Parasitologica Polonica 17, 65–87.Google Scholar
Harada, I (1938) Acanthocephalen aus Formosa. I. Annotationes Zoologicae Japanenses 17, 419–427.Google Scholar
Hasegawa, M, Kishino, H and Yano, T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.Google Scholar
Hassanine, RME-S (2006) Acanthocephalans from Red Sea fishes. Family Cavisomidae Meyer, 1932: the seasonal cycle of Diplosentis nudus (Harada, 1938) Pichlein & Cribb, 2001 in a definitive fish host, and a comment on Sclerocollum schmidt et Paperna, 1978. Acta Parasitologica 51, 123–129.Google Scholar
Huffman, DG and Bullock, WL (1975) Meristograms: graphical analysis of serial variation of proboscis hooks of Echinorhynchus (Acanthocephala). Systematic Zoology 24, 333–345.Google Scholar
Kartavtsev, YP (2011) Sequence divergence at mitochondrial genes in animals: applicability of DNA data in genetics of speciation and molecular phylogenetics. Marine Genomics 4, 71–81.Google Scholar
Král'ová-Hromadová, I, Tietz, DF, Shinn, AP and Spakulová, M (2003) ITS rDNA sequences of Pomphorhynchus laevis (Zoega in Müller, 1776) and P. lucyi williams & Rogers, 1984 (Acanthocephala: Palaeacanthocephala). Systematic Parasitology 56, 141–145.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, McGettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A, Lopez, R, Thompson, JD, Gibson, TJ and Higgins, DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 23, 2947–2948.Google Scholar
Li, W, Cowley, A, Uludag, M, Gur, T, McWilliam, H, Squizzato, S, Park, YM, Buso, N and Lopez, R (2015) The EMBL-EBI bioinformatics web and programmatic tools framework. Nucleic Acids Research 43, W580–W584.Google Scholar
Li, L, Chen, H-X, Amin, OM and Yang, Y (2017) Morphological variability and molecular characterization of Pomphorhynchus zhoushanensis sp. nov. (Acanthocephala: Pomphorhynchidae), with comments on the systematic status of Pomphorhynchus monticelli, 1905. Parasitology International 66, 693–698.Google Scholar
Li, L, Chen, H-X and Yang, Y (2018) Morphological and molecular study of Neorhadinorhynchus nudus (Harada, 1938) (Acanthocephala: Cavisomidae) from Auxis thazard Lacepede (Perciformes: Scombridae) in the South China Sea. Acta Parasitologica 63, 479–485.Google Scholar
Martínez-Aquino, A, Reyna-Fabián, ME, Rosas-Valdez, R, Razo-Mendivil, U, Ponce de León, G and García-Varela, M (2009) Detecting a complex of cryptic species within Neoechinorhynchus golvani (Acanthocephala: Neoechinorhynchidae) inferred from ITSs and LSU rDNA gene sequences. Journal of Parasitology 95, 1040–1047.Google Scholar
Mordvinova, TN (1988) Neorhadinorhynchus myctophumi (Acanthocephala), a new acanthocephalan species from Atlantic myctophid fish. Zoologičeskij Žurnal 67, 1411–1414, [In Russian].Google Scholar
Paradis, E (2010) Pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics (Oxford, England) 26, 419–420.Google Scholar
Petrochenko, V (1956) Acanthocephala of domestic and wild animals. 1. Izdatel'stvo Akademii Nauk SSSR, Moscow, 435 pp.Google Scholar
Pigliucci, M, Murren, CJ and Schlichting, CD (2006) Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology 209, 2362–2367.Google Scholar
Rice, P, Longden, I and Bleasby, A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends in Genetics 16, 276–277.Google Scholar
Ruse, M (1969) Definitions of species in biology. The British Journal for the Philosophy of Science 20, 97–119.Google Scholar
Schmidt, GD (1985) Development and life cycles. In Crompton, DWT and Nickol, BB (eds), Biology of the Acanthocephala. Cambridge: Cambridge University Press, pp. 273–286.Google Scholar
Shostak, AW, Dick, TA, Szalai, AJ and Bernier, LMJ (1986) Morphological variability in Echinorhynchus gadi, E. leidyi, and E. salmonis (acanthocephala: Echinorhynchidae) from fishes in northern Canadian waters. Canadian Journal of Zoology 64, 985–995.Google Scholar
Smales, LR, Al-Hasson, HAH, Al-Niaeem, KS and Al-Azizz, SA (2015) A new species of Neorhadinorhynchus (Acanthocephala: Cavisomidae) from Platax teira (Ephippidae) from Iraqi marine waters. Transactions of the Royal Society of South Australia 140, 90–95.Google Scholar
Sobecka, E, Szostakowska, B, MacKenzie, K, Hemmingsen, W, Prajsnar, S and Eydal, M (2012) Genetic and morphological variation in Echinorhynchus gadi Zoega in Müller, 1776 (Acanthocephala: Echinorhynchidae) from Atlantic cod Gadus morhua L. Journal of Helminthology 86, 16–25.Google Scholar
Steinauer, ML, Nickol, BB and Ortí, G (2007) Cryptic speciation and patterns of phenotypic variation of a highly variable acanthocephalan parasite. Molecular Ecology 16, 4097–4109.Google Scholar
Templeton, AR, Crandall, KA and Sing, CF (1992) A cladistic analysis of phenotypic association with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–635.Google Scholar
Tkach, VV, Lisitsyna, OI, Crossley, JL, Binh, TT and Bush, SE (2013) Morphological and molecular differentiation of two new species of Pseudoacanthocephalus petrochenko, 1958 (Acanthocephala: Echinorhynchidae) from amphibians and reptiles in the Philippines, with identification key for the genus. Systematic Parasitology 85, 11–26.Google Scholar
Väinölä, R, Valtonen, ET and Gibson, DI (1994) Molecular systematics in the acanthocephalan genus Echinorhynchus (sensu lato) in northern Europe. Parasitology 108, 105–114.Google Scholar
Van Cleave, HJ (1953) Acanthocephala of North American Mammals. Illinois: University of Illinois Press, pp. 164.Google Scholar
Wayland, MT (2010) Proboscis profiler: a tool for detecting acanthocephalan morphotypes. Systematic Parasitology 76, 159–167.Google Scholar
Yamaguti, S (1939) Studies on the helminth fauna of Japan Part 29. Acanthocephala, II. Japanese Journal of Zoology 8, 317–351.Google Scholar
Yamaguti, S (1963) Systema Helminthum, Vol. V. Acanthocephala. New York, London: Interscience Publishers, 423 pp.Google Scholar