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Deep in the systematics of Camallanidae (Nematoda): using integrative taxonomy to better understand the phylogeny and consistency of diagnostic traits

Published online by Cambridge University Press:  03 May 2021

Lorena G. Ailán-Choke
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Instituto para el Estudio de la Biodiversidad de Invertebrados, Facultad de Ciencias Naturales, Universidad Nacional de Salta, Av. Bolivia 5150, 4400 Salta, Argentina
Felipe B. Pereira*
Affiliation:
Department of Parasitology, Institute of Biological Sciences, Federal University of Minas Gerais, Av. Antonio Carlos, 6627, Pampulha, CEP 31270-901, Belo Horizonte, MG, Brazil
*
Author for correspondence: Felipe B. Pereira, E-mail: felipebisaggiop@hotmail.com

Abstract

Due to conflicts between classic and molecular systematics of Camallanidae, different data types were used for the first time, to better understand the evolutionary history and taxa consistency within this family. Genetic [18S and 28S rDNA; cytochrome c oxidase subunit I (COI) mtDNA], morphological and life history traits were used to infer phylogenies using Bayesian inference, reconstructed from separated and concatenated datasets. The consistency of tree and morphological traits was evaluated using the consistency index. Characters were mapped on the trees and the phylogenetic informativeness of genetic markers was estimated. Phylogenetic informativeness of 18S provided better resolution for outer nodes, COI for inners and 28S had an intermediate profile. New sequences for two camallanid species were obtained. Phylogenies of genetic and concatenated data largely agreed, showing more divergence in the COI dataset, due to its higher mutation rate vs stable morphology for diagnosing higher taxa. No genus sustained monophyly. The lack of autapomorphy and phylogenetic proximity supported the partition of Batrachocamallanus as synonym of Procamallanus and Spirocamallanus, which should not be considered as subgenera. Although traits of buccal capsule, male tail, habitat, host and biogeographic were highly consistent, intrinsic patterns varied according to different taxa assemblages. Morphological systematics of Camallanidae, based on buccal capsule, is artificial for certain taxa.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Ailán-Choke, LG, Ramallo, G and Davies, D (2018) Further study on Procamallanus (Spirocamallanus) pintoi (Kohn et Fernandes, 1988) (Nematoda: Camallanidae) in Corydoras paleatus and Corydoras micracanthus (Siluriformes: Callichthyidae) from Salta, Argentina, with a key to congeneric species from Neotropical realm. Acta Parasitologica 63, 595604.CrossRefGoogle Scholar
Ailán-Choke, LG, Davies, DA, Tavares, LER and Pereira, FB (2019) An integrative taxonomic assessment of Procamallanus (Spirocamallanus) huacraensis (Nematoda: Camallanidae), infecting the freshwater catfish Trichomycterus spegazzinii (Siluriformes: Trichomycteridae) in Argentina. Parasitology Research 118, 28192829.CrossRefGoogle Scholar
Ailán-Choke, LG, Tavares, LER, Luque, JL and Pereira, FB (2020) An integrative approach assesses the intraspecific variations of Procamallanus (Spirocamallanus) inopinatus, a common parasite in neotropical freshwater fishes, and the phylogenetic patterns of Camallanidae. Parasitology 147, 17521764.CrossRefGoogle ScholarPubMed
Allio, R, Donega, S, Galtier, N and Nabholz, B (2017) Large variation in the ratio of mitochondrial to nuclear mutation rate across animals: implications for genetic diversity and the use of mitochondrial DNA as a molecular marker. Molecular Biology and Evolution 34, 27622772.CrossRefGoogle ScholarPubMed
Anderson, R, Chabaud, A and Willmott, S (2009) Keys to the Nematode Parasites of Vertebrates: Archival Volume. Wallingford: CABI Publishing.CrossRefGoogle Scholar
Betancur, RR, Wiley, EO, Arratia, G, Acero, A, Bailly, N, Miya, M, Lecointre, G and Ortí, G (2017) Phylogenetic classification of bony fishes. BMC Evolutionary Biology 17, 140.CrossRefGoogle Scholar
Blasco-Costa, I, Rouco, C and Poulin, R (2015) Biogeography of parasitism in freshwater fish: spatial patterns in hot spots of infection. Ecography 38, 301310.CrossRefGoogle Scholar
Bouckaert, RR and Drummond, AJ (2017) bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology 17, 111.CrossRefGoogle ScholarPubMed
Bouckaert, R, Vaughan, TG, Barido-Sottani, J, Duchêne, S, Fourment, M, Gavryushkina, A, Heled, J, Jones, G, Kühnert, D, De Maio, N, Matschiner, M, Mendes, FK, Müller, NF, Ogilvie, HA, Du Plessis, L, Popinga, A, Rambaut, A, Rasmussen, D, Siveroni, I, Suchard, MA, Wu, CH, Xie, D, Zhang, C, Stadler, T and Drummond, AJ (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 15, 128.CrossRefGoogle ScholarPubMed
Černotíková, E, Horák, A and Moravec, F (2011) Phylogenetic relationships of some spirurine nematodes (Nematoda: Chromadorea: Rhabditida: Spirurina) parasitic in fishes inferred from SSU rRNA gene sequences. Folia Parasitologica 58, 135148.CrossRefGoogle ScholarPubMed
Chabaud, AG and Bain, O (1994) The evolutionary expansion of the Spirurida. International Journal for Parasitology 24, 11791201.CrossRefGoogle ScholarPubMed
Chabaud, AG and Brygoo, ER (1962) Nématodes parasites de caméléons malgaches. Deuxième note. Annales de Parasitologie Humaine et Comparee 37, 569602.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
De, NC and Moravec, F (1980) Redescription of the nematode Procamallanus spiculogubernaculus with notes on related forms. Věstník Československé Zoologické Společnosti 44, 8191.Google Scholar
Froese, R and Pauly, D (eds) (2021) FishBase. World Wide Web electronic publication. Available at http://www.fishbase.org (accessed 04/2021).Google Scholar
Frost, DR (2021) Amphibian Species of the World: an Online Reference. Version 6.1. World Wide Web electronic publication.Google Scholar
Gomez-Puerta, L, Carrasco, J, Lopez-Urbina, M and Gonzalez, A (2018) Morphological and molecular identification of Spirocerca lupi (Nematoda: Spiruridae) found in the Andean fox (Lycalopex culpaeus). Journal of Parasitic Diseases 42, 449454.CrossRefGoogle Scholar
Harnoster, F, Svitin, R and Preez, LD (2019) Serpinema cayennensis n. sp. (Nematoda: Camallanidae), a parasite of the freshwater turtle Rhinoclemmys punctularia Daudin (Reptilia: Testudines: Geoemydidae) from French Guiana: morphology and phylogenetic relationships with other turtle-parasitising camallanids. Zootaxa 4679, 1.11.CrossRefGoogle Scholar
Hasegawa, H, Williams, EH and Bunkley-Williams, L (1991) Nematode parasites from marine fishes of Okinawa, Japan. Journal of the Helminthological Society of Washington 58, 186197.Google Scholar
Hernández-Lara, C, Espinosa de los Monteros, A, Ibarra-Cerdeña, CN, García-Feria, L and Santiago-Alarcon, D (2018) Combining morphological and molecular data to reconstruct the phylogeny of avian Haemosporida. International Journal for Parasitology 48, 11371148.CrossRefGoogle ScholarPubMed
Hughes, LC, Orti, G, Huang, Y, Sun, Y, Baldwin, CC, Thompson, AW, Arcila, DR, Li, CH, Becker, L, Bellora, N, Zhao, XM, Li, XF, Wang, M, Fang, C, Xie, B, Zhou, ZC, Huang, H, Chen, SL, Venkatesh, B and Shi, Q (2018) Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data. Proceedings of the National Academy of Sciences 115, 62496254.CrossRefGoogle ScholarPubMed
Ivashkin, VM, Sobolev, AA and Khromova, LA (1971) Camallanata of Animals and Man and The Diseases Caused by Them. Moskva: Nauka.Google Scholar
Jackson, JA and Tinsley, RC (1995) Representatives of Batrachocamallanus n. g. (Nematoda: Procamallaninae) from Xenopus spp. (Anura: Pipidae): geographical distribution, host range and evolutionary relationships. Systematic Parasitology 31, 159188.CrossRefGoogle Scholar
Kern, EMA, Kim, T and Park, JK (2020) The mitochondrial genome in nematode phylogenetics. Frontiers in Ecology and Evolution 8, 250.CrossRefGoogle Scholar
Kimura, M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.CrossRefGoogle ScholarPubMed
Kocsis, ÁT, Reddin, CJ and Kiessling, W (2018) The stability of coastal benthic biogeography over the last 10 million years. Global Ecology and Biogeography 2018, 11061120.CrossRefGoogle Scholar
Kohn, A and Fernandes, BMN (1987) Estudo comparativo dos helmintos parasitos de peixes do Rio Mogi Guassu, coletados nas excursoes realizadas entre 1927 e 1985. Memórias do Instituto Oswaldo Cruz 82, 483500.CrossRefGoogle Scholar
Kuzmin, Y, Tkach, VV, Snyder, SD and Maier, MD (2009) Camallanus tuckeri n. sp. (Nematoda: Camallanidae) from freshwater turtles (Pleurodira: Chelidae), in the Kimberley, Western Australia. Comparative Parasitology 76, 133140.CrossRefGoogle Scholar
Kuzmin, Y, Tkach, VV, Snyder, SD and Bell, JA (2011) Camallanus Railliet et Henry, 1915 (Nematoda, Camallanidae) from Australian freshwater turtles with descriptions of two new species and molecular differentiation of known taxa. Acta Parasitologica 56, 213226.CrossRefGoogle Scholar
Lewis, PO (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50, 913925.CrossRefGoogle ScholarPubMed
Maddison, WP and Maddison, D (2019) Mesquite. Available from: www.gnu.org.Google Scholar
Malta, LS, Paiva, F, Elisei, C, Tavares, LER and Pereira, FB (2020) Integrative taxonomy of Sprentascaris mahnerti and phylogeny of raphidascaridid nematodes (Nematoda: Ascaridoidea: Raphidascarididae) suggest the monophyly of Sprentascaris. Parasitology International 74, 101978.CrossRefGoogle ScholarPubMed
Moravec, F (1969) Observations on the development of Camallanus lacustris. Věstník Československé Společnosti Zoologické 33, 1533.Google Scholar
Moravec, F (1998) Nematodes of Freshwater Fishes of the Neotropical Region. Praha: Academia.Google Scholar
Moravec, F and Justine, J-L (2006) Camallanus cotti (Nematoda: Camallanidae), an introduced parasite of fishes in New Caledonia. Folia Parasitologica 53, 287296.CrossRefGoogle Scholar
Moravec, F and Justine, J-L (2011) New data on the morphology of Procamallanus (Procamallanus) annulatus and Procamallanus (Spirocamallanus) monotaxis (Nematoda: Camallanidae) from marine fishes off New Caledonia. Helminthologia 48, 4150.CrossRefGoogle Scholar
Moravec, F and Nagasawa, K (1989) Observations on some nematodes parasitic in Japanese freshwater fishes. Folia Parasitologica 36, 127141.Google Scholar
Moravec, F and Sey, O (1988) Nematodes of freshwater fishes. Part. I. Camallanoidea and Habronematoidea. Věstník Ceskoslovenské Společnosti Zooligiské 52, 128148.Google Scholar
Moravec, F and Thatcher, VE (1997) Procamallanus (Denticamallanus subgen. n.) dentatus sp. n. (Nematoda, Camallanidae) from the characid fish, Bryconops alburnoides, in the Brazilian Amazon. Parasite 4, 239243.CrossRefGoogle Scholar
Moravec, F and Van As, LL (2015) Procamallanus (Spirocamallanus) spp. (Nematoda: Camallanidae) from fishes of the Okavango River, Botswana, including P. (S.) serranochromis n. sp. parasitic in Serranochromis spp. (Cichlidae). Systematic Parasitology 90, 151164.CrossRefGoogle Scholar
Moravec, F, Nie, P and Wang, G (2003) Some nematodes of fishes from central China, with the redescription of Procamallanus (Spirocamallanus) fulvidraconis (Camallanidae). Folia Parasitologica 50, 220230.CrossRefGoogle Scholar
Moravec, F, Nie, P and Wang, G (2004) Redescription of Camallanus hypophthalmichthys (Nematoda Camallanidae) and its first record from fishes in China. Journal of Parasitology 90, 14631467.CrossRefGoogle ScholarPubMed
Moravec, F, Justine, J-L, Würtz, J, Taraschewski, H and Sasal, P (2006) A new species of Procamallanus (Nematoda: Camallanidae) from Pacific eels (Anguilla spp.). Journal of Parasitology 92, 130137.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Olson, DM, Dinerstein, E, Wikramanayake, ED, Burgess, ND, Powell, GVN, Underwood, EC, D'Amico, JA, Itoua, I, Strand, HE, Morrison, JC, Loucks, CJ, Allnutt, TF, Ricketts, TH, Kura, Y, Lamoreux, JF, Wettengel, WW, Hedao, P and Kenneth, RK (2001) Terrestrial ecoregions of the world: a new map of Ufe on Earth. BioScience 51, 933938.CrossRefGoogle Scholar
Pereira, FB and Luque, JL (2017) An integrated phylogenetic analysis on ascaridoid nematodes (Anisakidae, Raphidascarididae), including further description and intraspecific variations of Raphidascaris (Sprentascaris) lanfrediae in freshwater fishes from Brazil. Parasitology International 66, 898904.CrossRefGoogle ScholarPubMed
Pereira, FB, Luque, JL and Tavares, LER (2018) Integrative approach on Pharyngodonidae (Nematoda: Oxyuroidea) parasitic in reptiles: relationship among its genera, importance of their diagnostic features, and new data on Parapharyngodon bainae. PLoS ONE 13, e0200494.CrossRefGoogle ScholarPubMed
Pérez-Ponce de León, G and Choudhury, A (2015) Biogeography of helminth parasites of freshwater fishes in Mexico: the search for patterns and processes. Journal of Biogeography 32, 645659.CrossRefGoogle Scholar
Petter, AJ (1979) Essai de classification de la sousfamille des Procamallaninae (Nematoda, Camallanidae). Bulletin du Muséum National d'Histoire Naturelle. Section A. Zoologie 1, 9911008.Google Scholar
Pinto, RM, Fábio, SP, Noronha, D and Rolas, FJT (1974) Procamallanus brasileiros-Parte I (Nematoda, Camallanoidea). Memórias do Instituto Oswaldo Cruz 72, 205211.CrossRefGoogle Scholar
Puillandre, N, Lambert, A, Brouillet, S and Achaz, G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21, 18641877.CrossRefGoogle ScholarPubMed
Ramallo, G and Ailán-Choke, LG (2017) Observations on two Procamallanus (Spirocamallanus) species (Nematoda: Camallanidae) from freshwater fishes in Argentina, including description of Procamallanus (Spirocamallanus) juana sp. nov. Zootaxa 4323, 286294.CrossRefGoogle Scholar
Rambaudt, A, Drummond, AJ, Xie, D, Baele, G and Suchard, MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901CrossRefGoogle Scholar
Rigby, MC and Adamson, ML (1997) Spirocamallanus species of French Polynesian coral reef fishes. Canadian Journal of Zoology 75, 12701279.CrossRefGoogle Scholar
Rigby, MC, Font, WF and Deardorff, TL (1997) Redescription of Camallanus cotti Fujita, 1927 (Nematoda: Camallanidae) from Hawai'i. Journal of Parasitology 83, 11611164.CrossRefGoogle ScholarPubMed
Rigby, MR, Sharma, S, Hechinger, RF, Platt, TR and Weaver, JC (2008) Two new species of Camallanus (Nematoda: Spirurida: Camallanidae) from freshwater turtles in Queensland, Australia. Journal of Parasitology 94, 13641370.CrossRefGoogle ScholarPubMed
Rindoria, NM, Dos Santos, QM and Avenant-Oldewage, A (2020) Additional morphological features and molecular data of Paracamallanus cyathopharynx (Nematoda: Camallanidae) infecting Clarias gariepinus (Actinopterygii: Clariidae) in Kenya. Journal of Parasitology 106, 157166.CrossRefGoogle Scholar
Rohde, K (2002) Ecology and biogeography of marine parasites. Advances in Marine Biology 43, 186.CrossRefGoogle ScholarPubMed
Russel, PM, Brewer, BJ, Klaere, S and Bouckaert, RR (2019) Model selection and parameter inference in phylogenetics using nested sampling. Systematic Biology 68, 219233.CrossRefGoogle ScholarPubMed
Sardella, CJ, Pereira, FB and Luque, JL (2017) Redescription and first genetic characterisation of Procamallanus (Spirocamallanus) macaensis Vicente & Santos 1972 (Nematoda: Camallanidae), including re-evaluation of the species of Procamallanus (Spirocamallanus) from marine fishes off Brazil. Systematic Parasitology 94, 657668.CrossRefGoogle ScholarPubMed
Sayad, S and Yassin, A (2019) Quantifying the extent of morphological homoplasy: a phylogenetic analysis of 490 characters in Drosophila. Evolution Letters 3, 286298.CrossRefGoogle ScholarPubMed
Sharma, RSK, Rigby, MC, Sumita, S, Sani, RA, Vidyadaran, MK, Jasni, S and Dailey, MD (2002) Redescription of Serpinema octorugatum (Baylis, 1933) (Nematoda: Camallanidae) from the Malayan box turtle Cuora amboinensis (Daudin) (Chelonia: Bataguridae). Systematic Parasitology 53, 1928.CrossRefGoogle Scholar
Stromberg, PC, Shegog, JH and Crites, JL (1973) A description of the male and redescription of the female of Camallanus oxycephalus Ward and Magath, 1916 (Nematoda: Camallanidae). Proceedings of the Helminthological Society of Washington 40, 234237.Google Scholar
Svitin, R, Schoeman, AL and du Preez, LH (2018) New information on morphology and molecular data of camallanid nematodes parasitising Xenopus laevis (Anura: Pipidae) in South Africa. Folia Parasitologica 65, 003.CrossRefGoogle ScholarPubMed
Svitin, R, Truter, M, Kudlai, O, Smit, NJ and du Preez, L (2019) Novel information on the morphology, phylogeny and distribution of camallanid nematodes from marine and freshwater hosts in South Africa, including the description of Camallanus sodwanaensis n. sp. International Journal for Parasitology: Parasites and Wildlife 10, 263273.Google ScholarPubMed
Swofford, DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony. Sunderland, MA: Sinauer Associates, Version 4.0b.Google Scholar
Townsend, JP (2007) Profiling phylogenetic informativeness. Systematic Biology 56, 222231.CrossRefGoogle ScholarPubMed
Uetz, P, Freed, P and Hosek, J (eds) (2020) The Reptile Database. World Wide Web electronic publication. http://www.reptile-database.org (accessed 13 April 2021).Google Scholar
van der Wal, C, Ahyong, ST, Ho, SYW, Lins, LSF and Lo, N (2019) Combining morphological and molecular data resolves the phylogeny of Squilloidea (Crustacea: Malacostraca). Invertebrate Systematics 33, 89100.Google Scholar
Wijová, M, Moravec, F, Horák, A and Lukeš, J (2006) Evolutionary relationships of Spirurina (Nematoda: Chromadorea: Rhabditida) with special emphasis on dracunculoid nematodes inferred from SSU rRNA gene sequences. International Journal for Parasitology 36, 10671075.CrossRefGoogle ScholarPubMed
Xia, X (2018) DAMBE 7: new and improved tools for data analysis in molecular biology and evolution. Molecular Biology and Evolution 35, 15501552.CrossRefGoogle Scholar
Xia, X, Xie, Z and Li, WH (2003) Effects of GC content and mutational pressure on the lengths of exons and coding sequences. Journal of Molecular Evolution 56, 362370. https://doi.org/10.1007/s00239-002-2406-1.CrossRefGoogle ScholarPubMed
Yamaguti, S (1935) Studies on the helminth fauna of Japan. Part 9. Nematodes of fishes, 1. Japan. Journal of Zoology 6, 337386.Google Scholar
Zar, JH (2010) Biostatistical Analysis. Englewood Cliffs: Prentice Hall.Google Scholar
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