Abstract
The genus Rhabdochona includes more than 100 species infecting freshwater fishes in all zoogeographical regions of the world. In Mexico, 12 nominal species of Rhabdochona have been recorded. Of these, Rhabdochona ictaluri was originally described as a parasite of endemic catfishes of the family Ictaluridae; however, the species was later considered on morphological grounds as a junior synonym of Rhabdochona kidderi. In this study, newly sampled specimens of R. ictaluri were obtained from the type host and type locality and were used to perform a detailed morphological analysis and molecular phylogenetic inferences through one mitochondrial and two nuclear genes; data were used in an integrative taxonomy context to test the taxonomic status of R. ictaluri. This approach proved to be very useful to confirm the validity of this species, and robust species limits were established between these two putative species considering morphology, molecular data, host association, and biogeography.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguilar-Aguilar R, Rosas-Valdez R, Pérez-Ponce de León G (2010) Rhabdochona ictaluri sp. nov. (Nematoda, Rhabdochonidae) from ictalurid catfishes in Mexico. Acta Parasitol 55:276–280. https://doi.org/10.2478/s11686-010-0035-1
Agustí CF, Aznar J, Raga A (2005) Tetraphyllidean plerocercoids from western Mediterranean cetaceans and other marine mammals around the world: a comprehensive morphological analysis. J Parasitol 91:83–92. https://doi.org/10.1645/GE-372R
Albrecht GH (1980) Multivariate analysis and the study of form, with special reference to canonical variate analysis. Am Zool 20:679–693. https://doi.org/10.1093/icb/20.4.679
Alcántar-Escalera FJ, García-Varela M, Vázquez-Domínguez E, Pérez-Ponce de León G (2013) Using DNA barcoding to link cystacanths and adults of the acanthocephalan Polymorphus brevis in central Mexico. Mol Ecol Res 13:1116–1124. https://doi.org/10.1111/1755-0998.12090
Archidona-Yuste A, Navas-Cortés JA, Cantalapiedra-Navarrete C, Palomares-Rius JE, Castillo P (2016) Cryptic diversity and species delimitation in the Xiphinema americanum-group complex (Nematoda: Longidoridae) as inferred from morphometrics and molecular markers. Zool J Linnean Soc 176(2):231–265. https://doi.org/10.1111/zoj.12316
Blouin M (1998) Mitochondrial DNA, diversity in nematodes. J Helminthol 72:285–289. https://doi.org/10.1017/S0022149X00016618
Blouin M (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int J Parasitol 32:527–531. https://doi.org/10.1016/S0020-7519(01)00357-5
Casiraghi M, Anderson TJC, Bandi C, Bazzocchi C, Genchi C (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122:93–103. https://doi.org/10.1017/S0031182000007149
Caspeta-Mandujano JM (2010) Nemátodos parásitos de peces de agua dulce de México. AGT Editor, México
Chaudhary A, Kansal G, Singh N, Shobhna K, Verma M, Singh H (2017) Molecular identification of Thelandros scleratus and Thelastoma icemi (Nematoda: Oxyruida) using mitochondrial cox 1 sequences. Acta Parasitol 62:382–385. https://doi.org/10.1515/ap-2017-0045
Cheng QQ, Li D, Ma L (2005) Morphological differences between close populations discernible by multivariate analysis: a case study of genus Coilia (Teleostei: Clupeiformes). Aquat Living Resour 18:187–192. https://doi.org/10.1051/alr:2005020
Choudhury A, Nadler SA (2018) Phylogenetic relationships of spiruromorph nematodes (Spirurina: Spiruromorpha) in North American freshwater fishes. J Parasitol 104:496–504. https://doi.org/10.1645/17-195
Choudhury A, García-Varela M, Pérez-Ponce de León G (2017) Parasites of freshwater fishes and the Great American Biotic Interchange: a bridge too far? J Helminthol 91:174–196. https://doi.org/10.1017/S0022149X16000407
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristcs and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85:407–415. https://doi.org/10.1111/j.1095-8312.2005.00503.x
De Borba RS, da Silva EL, Pacheco ACS, Parise-Maltempi PP, Alves AL (2012) Trends in the kariotypic evolution of the Neotropical catfish family Heptapteridae Bockmann 1998 (Teleostei: Siluriformes). Rev Fish Biol Fisher 22:509–518. https://doi.org/10.1007/s11160-011-9245-3
De Ley P, Felix MA, Frisse LM, Nadler SA, Sternberg PW, Thomas WK (1999) Molecular and morphological characterization of two reproductively isolated species with mirror-image anatomy (Nematoda: Cephalobidae). Nematology 1:591–612. https://doi.org/10.1163/156854199508559
De Ley P, De Ley IT, Morris K, Abebe E, Mundo-Ocampo M, Yoder M, Heras J, Waumann D, Rocha-Olivares A, Burr AHJ, Baldwin JG, Thomas WK (2005) An integrated approach to fast and informative morphological vouchering of nematodes for applications in molecular barcoding. Phil Trans R Soc B 360:1945–1958. https://doi.org/10.1098/rstb.2005.1726
De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886. https://doi.org/10.1080/10635150701701083
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Heled J, Kearse M, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2010) Geneious, version 5.0.4. http://www.geneious.com. Accessed Jan 2018
Eberhardt UA (2010) Constructive step towards selecting a DNA barcode for Fungi. New Phytol 187:265–268. https://doi.org/10.1111/j.1469-8137.2010.03329.x
Egan AN (2015) Species delimitation and recognition in the Pediomelum megalanthum complex (Fabaceae) via multivariate morphometrics. PhytoKeys 44:65–87. https://doi.org/10.3897/phytokeys.44.8750
García-Varela M, Nadler SA (2005) Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. J Parasitol 91:1401–1409. https://doi.org/10.1645/GE-523R.1
Garrido-Olvera L, García-Prieto L, Pérez-Ponce de León G (2006) Checklist of the adult nematode parasites of fishes in freshwater localities from Mexico. Zootaxa 120:1–45. https://doi.org/10.11646/zootaxa.1201.1.1
Hawkins JA (2000) A survey of primary homology assessment: different botanists perceive and define characters in different ways. In: Scotland RW, Pennington RT (eds) Homology & systematics: coding characters for phylogenetic analysis. Taylor & Francis, London, pp 22–53
Helfman GS, Collete BB, Facey DE, Bowen BW (2009) The diversity of fishes: biology, evolution, and ecology, 2nd edn. Wiley-Blackwell, Oxford
Huang D, Meier R, Todd P, Chou LM (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. J Mol Evol 66:167–174. https://doi.org/10.1007/s00239-008-9069-5
Janssen T, Karssen G, Topalovíc O, Coyne D, Bert W (2017) Integrative taxonomy of root-knot nematodes reveals multiple independent origins of mitotic parthenogenesis. PLoS One 12(3):e0172190. https://doi.org/10.1371/journal.pone.0172190
Lamothe-Argumedo R (1997) Manual de técnicas para preparar y estudiar los parásitos de animales silvestres. AGT Editor, México D. F
Martínez-Aquino A, Ceccarelli FS, Eguiarte LE, Pérez-Ponce de León G (2014) Do the historical biogeography and evolutionary history of the digenean Margotrema spp. across Central Mexico mirror those of their freshwater fish hosts (Goodeinae)? PLoS One 9:e101700. https://doi.org/10.1371/journal.pone.0101700
Mayden RL (1992) Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, Stanford
Mazur M, Klajbor K, Kielich M, Sowińska M, Romo A, Montserrat JM, Boratyński A (2010) Intra-specific differentiation of Juniperus phoenicea in the western Mediterranean region revealed in morphological multivariate analysis. Dendrobiology 63:21–31
McKay BD, Mays HL Jr, Wu Y, Li H, Yao C-t, Nishiumi I, Zou F (2013) An empirical comparison of character-based and coalescent-based approaches to species delimitation in a young avian complex. Mol Ecol 22:4943–4957. https://doi.org/10.1111/mec.12446
Meik JM, Schaack S, Flores-Villela O, Streicher JW (2018) Integrative taxonomy at the nexus of population divergence and speciation in insular speckled rattlesnakes. J Nat Hist 52:989–1016
Mejia-Madrid HH, Choudhury A, Perez-Ponce de Leon G (2007a) Phylogeny and biogeography of Rhabdochona Railliet, 1916 (Nematoda: Rhabdochonidae) species from the Americas. Syst Parasitol 67:1–18. https://doi.org/10.1007/s11230-006-9065-3
Mejia-Madrid HH, Vazquez-Dominguez E, Perez-Ponce de Leon G (2007b) Phylogeography and freshwater basins in Central Mexico: recent history as revealed by the fish parasite Rhabdochona lichtenfelsi (Nematoda). J Biogeogr 34:787–801. https://doi.org/10.1111/j.1365-2699.2006.01651.x
Miller RR, Minckley WL, Norris SM (2005) Freshwater fishes of Mexico. The University of Chicago Press, Chicago
Moravec F, Adlard R (2016) Redescription of Rhabdochona papuanensis (Nematoda: Thelazioidea), a parasite of rainbow fishes (Melanotaenia spp.); the first record of the species of Rhabdochona in Australia. Acta Parasitol 61:820–827. https://doi.org/10.1515/ap-2016-0114
Moravec F, Huffman DG (1988) Observations on the genus Rhabdochona Railliet, 1916 (Nematoda: Rhabdochonidae) from fishes of central Texas, with descriptions of two new subspecies. Folia Parasitol 35:341–351
Moravec F, Vivas-Rodríguez C, Scholz T, Vargas-Vázquez J, Mendoza-Franco E, González-Solís D (1995) Nematodes parasitic in fishes of cenotes (= sinkholes) of the Peninsula of Yucatan, Mexico. Part 1. Adults. Folia Parasitol 42:115–129
Moravec F, Salgado-Maldonado G, Gónzalez-Sólis G, Caspeta-Mandujano JM (2012) Host-parasite relationships of Rhabdochona kidderi Pearse, 1936 (Nematoda: Rhabdochonidae) in fishes of the Lacantún River in the Lacandon rain forest of Chiapas State, southern Mexico, with a key to Mexican species of Rhabdochona Raillet, 1916. Syst Parasitol 82:1–12. https://doi.org/10.1007/s11230-012-9342-2
Moravec F, Pachanawan A, Kamchoo K (2013) Rhabdochona (Rhabdochona) hypsibarbi n. sp. (Nematoda: Rhabdochonidae) from the freshwater cyprinid fish Hypsibarbus wetmorei (Smith) in Northeast Thailand. J Parasitol 99:297–302. https://doi.org/10.1645/12-32.1
Nadler SA, Pérez-Ponce de León G (2011) Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138:1688–1709. https://doi.org/10.1017/S003118201000168X
Nadler SA, Adams BJ, Lyons ET, DeLong RL, Melin SR (2000) Molecular and morphometric evidence for separate species of Uncinaria (Nematoda: Ancylostomatidae) in California sea lions and northern fur seals: hypothesis testing supplants verification. J Parasitol 86:1099–1106. https://doi.org/10.1645/0022-3395
Nakano T, Okamoto M, Ikeda Y, Hasegawa H (2006) Mitochondrial cytochrome c oxidase subunit 1 gene and nuclear rDNA regions of Enterobius vermicularis parasitic in captive chimpanzees with special reference to its relationship with pinworms in humans. Parasitol Res 100:51–57. https://doi.org/10.1007/s00436-006-0238-4
Padial JM, Miralles A, de la Riva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7:16. https://doi.org/10.1186/1742-9994-7-16
Pante E, Schoelinck C, Puillandre N (2015) From integrative taxonomy to species description: one step beyond. Syst Biol 64:152–160. https://doi.org/10.1093/sysbio/syu083
Pearse AS (1936) Parasites from Yucatan. Carnegie Inst Wash Publ 457:45–59
Pereira T, Fonseca G, Mundo-Ocampo M, Guilherme B, Rocha-Olivares A (2010) Diversity of free-living marine nematodes (Enoplida) from Baja California assessed by integrative taxonomy. Mar Biol 157:1665–1678. https://doi.org/10.1007/s00227-010-1439-z
Pérez-Ponce de León G, Choudhury A (2002) Adult endohelminth parasites of ictalurid fishes (Osteichthyes: Ictaluridae) in México: empirical evidence for biogeographical patterns. Comp Parasitol 69:10–19. https://doi.org/10.1654/1525-2647(2002)069[0010:AEPOIF]2.0.CO;2
Pérez-Ponce de León G, Choudhury A (2005) Biogeography of helminth parasites of freshwater fishes in Mexico: the search for patterns and processes. J Biogeogr 32:645–659. https://doi.org/10.1111/j.1365-2699.2005.01218.x
Pérez-Ponce de León G, Choudhury A (2010) Parasite inventories and DNA-based taxonomy: lessons from helminths of freshwater fishes in a megadiverse country. J Parasitol 96:236–244. https://doi.org/10.1645/GE-2239.1
Pérez-Ponce de León G, García-Varela M, Pinacho-Pinacho CD, Sereno-Uribe AL, Poulin R (2016) Species delimitation in trematodes using DNA sequences: middle-American Clinostomum as a case study. Parasitology 143:1773–1789. https://doi.org/10.1017/S0031182016001517
Pérez-Rodríguez R, Domínguez-Domínguez O, Doadrio I, Cuevas-García E, Pérez-Ponce de León G (2015) Comparative historical biogeography of three groups of Nearctic freshwater fishes across central Mexico. J Fish Biol 86:993–1105. https://doi.org/10.1111/jfb.12611
Quiroz-Martínez B, Salgado-Maldonado G (2013) Patterns of distribution of the helminth parasites of freshwater fishes of Mexico. PLoS One 8:e54787. https://doi.org/10.1371/journal.pone.0054787
Rambaut, A. (2012) FigTree v1.4. Available from http://tree.bio.ed.ac.uk/software/figtree/. Accessed Jan 2018
Rego AA (2000) Cestode parasites of Neotropical teleost freshwater fishes. In: Salgado-Maldonado G, García-Aldrete AN, Vidal-Martínez VM (eds) Metazoan parasites in the neotropics: a systematic and ecological perspective. Instituto de Biología, Universidad Nacional Autónoma de México, México, D. F., pp 135–154
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Rosas-Valdez R, Pérez-Ponce de León G (2008) Composición taxonómica de los helmintos parásitos de ictalúridos y heptaptéridos (Osteichthyes: Siluriformes) de México, con una hipótesis de homología biogeográfica primaria. Rev Mex Biodiv 79:473–499
Satler JD, Carstens BC, Hedin M (2013) Multilocus species delimitation in a complex of morphologically conserved trapdoor spiders (Mygalomorphae, Antrodiaetidae, Aliatypus). Syst Biol 62:805–823. https://doi.org/10.1093/sysbio/syt041
Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, Christian E, Crozier RH (2009) Integrative taxonomy: a multisource approach to exploring biodiversity. Annu Rev Entomol 55:421–438. https://doi.org/10.1146/annurev-ento-112408-085432
Sereno-Uribe AL, Pinacho-Pinacho CD, García-Varela M, Pérez-Ponce de León G (2013) Using mitochondrial and ribosomal DNA sequences to test the taxonomic validity of Clinostomum complanatum Rudolphi, 1814 in fish-eating birds and freshwater fishes in Mexico, with the description of a new species. Parasitol Res 112:2855–2870. https://doi.org/10.1007/s00436-013-3457-5
Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337. https://doi.org/10.1007/s13127-011-0056-0
Singh N, Chaudhary A, Singh HS (2015) Molecular phylogeny of nematodes (Oxyurida: Travassosinematidae) from orthoptera (Gryllotalpidae) inferred by mitochondrial cytochrome C oxidase subunit 1 gene. Bioinformation 11:343–347. https://doi.org/10.6026/97320630011343
Sites JW Jr, Marshall JC (2003) Delimiting species: a renaissance issue in systematic biology. Trends Ecol Evol 18:462–470. https://doi.org/10.1016/S0169-5347(03)00184-8
Solórzano-García B, Nadler SA, Pérez-Ponce de León G (2016) Pinworm diversity in free-ranging howler monkeys (Alouatta spp.) in Mexico: morphological and molecular evidence for two new Trypanoxyuris species (Nematoda: Oxyuridae). Parasitol Int 65:401–411. https://doi.org/10.1016/j.parint.2016.05.016
StatSoft Inc. (2005) STATISTICA (data analysis software system), version 7.1. http://www.statsoft.com. Accessed Feb 2018
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Templeton AR (1989) The meaning of species and speciation: A genetic perspective. In: Otte DD, Endler JA (eds) Speciation and its consequences. Sinauer Associates, Sunderland, pp 3–27
Thompson JD, Higgins HG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Will KP, Mishler BD, Wheeler QD (2005) The perils of DNA barcoding and the need for integrative taxonomy. Syst Biol 54:844–851. https://doi.org/10.1080/10635150500354878
Acknowledgments
We thank Jaime Guzmán, Ramón Valdez, and Saúl Montoya for their help during field work; Luis García for the loan of specimens of Rhabdochona ictaluri and R. kidderi deposited in the CNHE, and for providing helpful bibliographic references; Berenit Mendoza for the preparation of specimens for SEM, and Laura Márquez for support obtaining DNA sequences.
Funding
This project was partially funded by the program PAPIIT-UNAM IN218414 to GR and IN202617 to GPPL. OLC, AOSV, and DIHM wish to thank the Consejo Nacional de Ciencia y Tecnología (CONACyT) for granting scholarships to complete their graduate programs.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Simonetta Mattiucci
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Lagunas-Calvo, O., Santacruz, A., Hernández-Mena, D.I. et al. Taxonomic status of Rhabdochona ictaluri (Nematoda: Rhabdochonidae) based on molecular and morphological evidence. Parasitol Res 118, 441–452 (2019). https://doi.org/10.1007/s00436-018-6189-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-018-6189-8