New Species of Gyrodactylus von Nordmann, 1832 from Native Fish from Chiapas, Mexico, Studied by Morphology and Molecular Analyses
Three new species of Gyrodactylus von Nordmann, 1832 are described from Poeciliopsis hnilickai and Tlaloc labialis (syn. Profundulus candalarius and Profundulus labialis) from the state of Chiapas, Mexico. Gyrodactylus chiapaneco n. sp. is described from T. labialis. Gyrodactylus guatopotei n. sp. was found to infect P. hnilickai. Gyrodactylus tlaloci n. sp. is described from T. labialis. The new species were characterised morphologically (haptoral hooks) and molecularly (sequences of the Internal Transcribed Spacer region (ITS1-5.8S-ITS2) of rDNA).
During a survey in March 2017 in the state of Chiapas, individuals of Tlaloc labialis were collected by electrofishing from Arroyo Ojo de Agua and from Río Hondo, Ixtapa, Río Las Lajas and Poeciliopsis hnilickai from Río Hondo, Ixtapa and Río Cacao. Three new species of Gyrodactylus were found and are described herein based on morphological and genetic analysis.
Attachment hooks were excised and partially digested with a proteolytic solution to remove tissue enclosing the haptoral armature. Measurements and pictures of the haptoral hard structures were taken and were compared with other Gyrodactylus species found on poeciliids and profundulids. The bodies from which haptoral hook were removed were stored individually in 95% ethanol at − 20 °C for molecular analyses. Sequences of the Internal Transcribed Spacer region of rDNA were obtained for each species and were compared with 26 Gyrodactylus spp. The genetic divergence among species of Gyrodactylus was estimated using uncorrected “p” distances with the program MEGA.
The haptoral hook of Gyrodactylus chiapaneco n. sp. are similar to G. poeciliae from Venezuela; those from Gyrodactylus guatopotei n. sp. resemble the sclerites of G. turnbulli from Singapore and G. pictae from Trinidad, and the haptoral hooks of Gyrodactylus tlaloci n. sp. are comparable to those of G. pseudobullatarudis and G. zapoteco from Mexico; most of these parasites were described from poeciliid fishes, except G. zapoteco which was recently described from Profundulus oxacae from Oxaca, Mexico. The sequences of the three new species were aligned with sequences of 26 other Gyrodactylus spp. Maximum likelihood and Bayesian inference analyses indicated that the three new taxa are members with well-supported lineages—the new taxa are the first species of Gyrodactylus to be described from Poeciliopsis hnilickai and Tlaloc labialis from Chiapas.
Gyrodactylus chiapaneco n. sp., Gyrodactylus guatopotei n. sp. and Gyrodactylus tlaloci n. sp. are described based on morphological and molecular analyses. Two of the three new species of Gyrodactylus described here, and both roughly fall morphologically and molecularly into the group of parasites harbouring slender marginal hooks: G. chiapaneco n. sp. and G. tlaloci n. sp. both possess marginal sclerites with slim shafts and group phylogenetically with other gyrodactylids of similar marginal hook morphology. Gyrodactylus guatopotei n. sp. groups with gyrodactylids possessing marginal hooks with quite elongated shafts, most of which have been found infecting poeciliids in the Antilles (e.g. G. pictae and G. turnbulli). Poeciliid, profundulid and goodeid fishes are morphologically and ecologically similar and nowadays live in sympatry or close geographical distance in Mesoamerica.
KeywordsFreshwater fish Integrative taxonomy Mexico ITS Gyrodactylus
We thank the staff at Universidad de Ciencias y Artes de Chiapas, Tuxtla Gutiérrez, Chiapas for allowing us the use of facilities and for their help collecting fish in the field: Wilfredo Matamorros, Ernesto Velázquez Velázquez, Manuel J. Anzueto Calvo, Juan Anzueto Calvo, Ismael Aguilar Pérez and Jorge L. Lievano Trujillo. Thanks to Luis García-Prieto from the Colección Nacional de Helmintos (CNHE), Universidad Nacional Autónoma de México (UNAM) for the loan of Gyrodactylus type material. We also want to thank the two reviewers who very kindly took their time to review the manuscript. Field sampling was performed according to Mexican codes of practice and received approval of the Mexican Ministry of the Environment and Natural Resources, Secretaria de Medio Ambiente y Recursos Nturales (SEMARNAT) (permit no. FAUT-0105) to GSM.
GSM, MRG conceived and designed the study, AGV, CDPP, IGV collected the specimens and performed the morphological, structural and molecular analyses. All authors wrote the paper and approved the final version of the manuscript.
This research was supported by grant PAPIIT IN203016 awarded to Guillermo Salgado-Maldonado by Universidad Nacional Autónoma de México (UNAM), Dirección General de Asuntos del Personal Académico. AGV thanks INECOL for her postdoctoral fellowship.
- 1.Rodiles-Hernádez R (2005) Diversidad de peces continentales en Chiapas. In: González-Espinoza M, Ramírez-Marcial N, Ruíz-Montoya M (eds) Diversidad biológica de Chiapas. Plaza y Valdés, México, pp 141–160Google Scholar
- 4.Salgado-Maldonado G (2008) Helmitnh parasites of freshwater fish from Central America. Zootaxa 1915:29–53Google Scholar
- 7.Salgado-Maldonado G, Caspeta-Mandujano JM, Martínez-Ramírez E (2011) Paracreptotrema profundulusi n. sp. and P. blancoi Choudhury, Pérez Ponce de León, Brooks and Daverdin, 2006 (Trematoda: Allocreadiidae) from freshwater fishes of the genus Profundulus (Teleostei: Profundulidae) in Southern Mexico. J Parasitol 97:707–712. https://doi.org/10.1645/GE-2662.1 CrossRefGoogle Scholar
- 9.Pérez-Ponce de León G, Pinacho-Pinacho CD, Mendoza-Garfias B, García-Varela M (2015) Phyllodistomum spinopapillatum sp. nov. (Digenea: Gorgoderidae), from the Oaxaca killifish Profundulus balsanus (Osteichthyes: Profundulidae) in Mexico, with new host and locality records of P. inecoli: Morphology, ultrastructure and molecular evidence. Acta Parasitol 60:298–307. https://doi.org/10.1515/ap-2015-0042 Google Scholar
- 10.Pinacho-Pinacho CD, Pérez-Ruíz MA, Sereno-Uribe AL, García-Varela M, Martínez-Ramírez E (2014) Richness and similarity of helminth communities of the freshwater fish Profundulus punctatus (Pisces: Cyprinodontidae) from Oaxaca, Mexico. Rev Mex Biodivers 85:1129–1138. https://doi.org/10.7550/rmb.41776 CrossRefGoogle Scholar
- 11.Pinacho-Pinacho CD, García-Varela M, Hernández-Orts JS, Mendoza-Palmero CA, Sereno-Uribe AL, Martínez-Ramírez E, Andrade-Gómez L, López-Jiménez A, Hernández-Cruz E, Pérez-Ponce de León G (2015) Checklist of the helminth parasites of the genus Profundulus Hubbs, 1924 (Cyprinodontiformes, Profundulidae), an endemic family of freshwater fishes in Middle-America. ZooKeys 523:1–30. https://doi.org/10.3897/zookeys.523.6088 CrossRefGoogle Scholar
- 12.Salgado-Maldonado G, Matamoros WA, Caspeta-Mandujano JM, Martínez-Ramírez E, Mendoza-Franco E, Velázquez-Velázquez E (2014) Range extensión of helminth parasites of Profundulus spp. (Teleostei: Profundulidae) from Southern Mexico and Central America. Check List 10:1507–1513. https://doi.org/10.15560/10.6.1507 CrossRefGoogle Scholar
- 14.Velázquez-Velázquez E, Méndez-Gómez B, Salgado-Maldonado G, Matamoros W (2015) The invasive tapeworm Bothriocephalus acheilognathi Yamaguti, 1934 in the endangered killifish Profundulus candalarius Hubbs, 1924 in Chiapas, Mexico. BioInvasions Records 4:265–268. https://doi.org/10.3391/bir.2015.4.4.06 CrossRefGoogle Scholar
- 15.García-Vásquez A, Pinacho-Pinacho CD, Martínez-Ramírez E, Rubio-Godoy M (2018) Two new species of Gyrodactylus von Nordmann, 1832 from Profundulus oaxacae (Pisces: Profundulidae) from Oaxaca, Mexico, studied by morphology and molecular analyses. Parasitol Int 67:517–527. https://doi.org/10.1016/j.parint.2018.03.003 CrossRefGoogle Scholar
- 16.Morcillo F, Ornelas-García CP, Alcaraz L, Matamoros WA, Doadrio I (2016) Phylogenetic relationships and evolutionary history of the Mesoamerican endemic freshwater fish family Profundulidae (Cyprinodontiformes: Actinopterygii). Mol Phylogenet Evol 94:242–251. https://doi.org/10.1016/j.ympev.2015.09.002 CrossRefGoogle Scholar
- 17.Rubio-Godoy M, Razo-Mendivil U, García-Vásquez A, Freeman MA, Shinn AP, Paladini G (2016) To each his own: no evidence of gyrodactylid parasite host switches from invasive poeciliid fishes to Goodea atripinnis Jordan (Cyprinodontiformes: Goodeidae), the most dominant endemic freshwater goodeid fish in the Mexican Highlands. Parasites Vectors 9:604. https://doi.org/10.1186/s13071-016-1861-2 CrossRefGoogle Scholar
- 19.García-Vásquez A, Razo-Mendivil U, Rubio-Godoy M (2015) Morphological and molecular description of eight new species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogenea) from poeciliid fishes, collected in their natural distribution range in the Gulf of Mexico slope, Mexico. Parasitol Res 114:3337–3355. https://doi.org/10.1007/s00436-015-4559-z CrossRefGoogle Scholar
- 21.Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
- 24.Ronquist F, Teslenko M, van der Mark P, Ayres D, 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 CrossRefGoogle Scholar
- 25.Rambaut A (2006) FigTree v1.3.1. University of Edinburgh, EdinburghGoogle Scholar
- 27.Shinn AP, Harris PD, Cable J, Bakke TA, Paladini G, Bron JE (2011) GyroDb World Wide Web electronic publication. http://www.gyrodb.net. Accessed 16 May 2019
- 29.Miller RR, Minckley WL, Norris SM (2005) Freshwater fishes of Mexico. The University of Chicago Press, ChicagoGoogle Scholar
- 31.Miller RR (1955) A systematic review of the middle American fishes of the genus Profundulus. Misc Publ Mus Zool Univ Mich 92:1–64Google Scholar
- 32.Doadrio I, Carmona JA, Martínez E, De Sostoa-Fernández A (1999) Genetic variation and taxonomic analysis of the subgenus Profundulus. J Fish Biol 55:751–766. https://doi.org/10.1111/j.1095-8649.1999.tb00715.x CrossRefGoogle Scholar
- 33.Miller R (2005) Freshwater fishes of Mexico, vol 1. The University of Chicago Press, ChicagoGoogle Scholar
- 36.Rubio-Godoy M, Paladini G, García-Vásquez A, Shinn AP (2010) Gyrodactylus jarocho sp. nov. and Gyrodactylus xalapensis sp. nov. (Platyhelminthes: Monogenea) from Mexican poeciliids (Teleostei: Cyprinodontiformes), with comments on the known gyrodactylid fauna unfecting poeciliid fish. Zootaxa 2509:1–29. https://doi.org/10.11646/%25x CrossRefGoogle Scholar
- 37.Mendoza-Palmero CA, Sereno-Uribe AL, Salgado-Maldonado G (2009) Two new species of Gyrodactylus von Nordmann, 1832 (Monogenea: yrodactylidae) parasitizing Girardinichthys multirradiatus (Cyprinodontiformes: Goodeidae), an endemic freshwater fish from Central Mexico. J Parasitol 9:315–318. https://doi.org/10.1016/j.parint.2018.03.003 CrossRefGoogle Scholar
- 38.Huyse T, Audenaert V, Volckaert FA (2003) Speciation and host–parasite relationships in the parasite genus Gyrodactylus (Monogenea, Platyhelminthes) infecting gobies of the genus Pomatoschistus (Gobiidae, Teleostei). Int J Parasitol 33:1679–1689. https://doi.org/10.1016/S0020-7519(03)00253-4 CrossRefGoogle Scholar
- 39.Ziętara MS, Arndt A, Geets A, Hellemans B, Volckaert FA (2000) The nuclear rDNA region of Gyrodactylus arcuatus and G. branchicus (Monogenea: Gyrodactylidae). J Parasitol 86:1368–1373. https://doi.org/10.1645/0022-3395(2000).086%5b1368:TNRROG%5d2.0.CO;2 CrossRefGoogle Scholar
- 40.Ziętara MS, Kuusela J, Veselov A, Lumme J (2008) Molecular faunistics of accidental infections of Gyrodactylus Nordmann, 1832 (Monogenea) parasitic on salmon Salmo salar L. and brown trout Salmo trutta L. in NW Russia. Syst Parasitol 69:123–135. https://doi.org/10.1007/s11230-007-9121-7 CrossRefGoogle Scholar
- 42.Hansen H, Jørgensen A, Mo TA (2012) Spin-off from routine parasite diagnostics of Atlantic salmon; first report of Gyrodactylus alexanderi in Norway. Bull Eur Assoc Fish Pathol 32:14–18Google Scholar
- 43.Cable J, Van Oosterhout C, Barson N, Harris PD (2005) Gyrodactylus pictae n. sp. (Monogenea: Gyrodactylidae) from the Trinidadian swamp guppy Poecilia picta Regan, with a discussion on species of Gyrodactylus von Nordmann, 1832 and their poeciliid hosts. Syst Parasitol 60:159–164. https://doi.org/10.1007/s11230-004-6348-4 CrossRefGoogle Scholar
- 46.García-Vásquez A, Guzmán-Valdivieso I, Razo-Mendivil U, Rubio-Godoy M (2018) Three new species of Gyrodactylus von Nordmann, 1832 described from Goodea atripinnis (Pisces: Goodeidae), an edemic freshwater fish from the central highlands of Mexico. Parasitol Res 117:139–150. https://doi.org/10.1007/s00436-017-5680-y CrossRefGoogle Scholar
- 47.Razo-Mendivil U, García-Vásquez A, Rubio-Godoy M (2016) Spot the difference: two cryptic species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogenea) infecting Astyanax aeneus (Actinopterygii, Characidae) in Mexico. Parasitol Int 65:398–400. https://doi.org/10.1016/j.parint.2016.05.009 CrossRefGoogle Scholar
- 48.King SD, Cone DK (2009) Morphological and molecular taxonomy of a new species of Fundulotrema and comments on Gyrodactylus stephanus (Monogenea: Gyrodactylidae) from Fundulus heteroclitus (Actinopterygii: Cyprinodontiformes) in Nova Scotia, Canada. J Parasitol 95:846–849. https://doi.org/10.1645/GE-1901.1 CrossRefGoogle Scholar