The high morphological variation found in the immature stages of the nematode Gnathostoma sp. I is not supported by molecular information

Authors

DOI:

https://doi.org/10.22201/ib.20078706e.2025.96.5098

Keywords:

Gnathostoma spp., Advanced third stage, Phylogeny, Mexico, Marsupials

Abstract

The third-stage advanced larvae (AdvL3) of Gnathostoma sp. I isolated from the musculature of Dormitator latifrons and Rhamdia guatemalensis are identical to each other morphological and molecularly, and are genetically related to a juvenile isolated from the liver of Didelphis marsupialis, in the Ostuta River basin, Oaxaca. They are different from the 3 species of Gnathostoma described from Mexico by body size and the hooks of the cephalic bulb in the AdvL3 stage, as well as, in the presence of a cuticular pouch at the posterior end of the juvenile male. Through the COI molecular marker, a genetic distance analysis, and phylogenetic inference among the species of the genus, we conclude that Gnathostoma sp. I is closely related to, but distinct from G. turgidum and from other species found in Mexico and worldwide, even though there is not enough material to establish it as a new species. Additionally, based on morphologic characteristics, we documented the discovery of AdvL3 of G. lamothei (in Rhambdia guatemalensis and Lontra longicaudis) and AdvL3 of another unidentified species (in R. guatemalensis and Synbranchus marmoratus), which is distinct to above according to morphologic and molecular evidence.

References

Almeyda-Artigas, R. J. (1991). Hallazgo de Gnathostoma binucleatum n. sp. (Nematoda: Spirurida) en felinos silvestres y el papel de peces dulceacuícolas y oligohalinos como vectores de la gnathostomiasis humana en la cuenca baja del río Papaloapan, Oaxaca-Veracruz, México. Anales del Instituto Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, 18, 137–155.

Almeyda-Artigas, R. J., Bargues, M. D. y Mas-Coma, S. (2000a). ITS-2 rDNA sequencing of Gnathostoma species (Nematoda) and elucidation of the species causing human gnathostomiasis in the Americas. Journal of Parasitology, 86, 537–544. https://doi.org/10.1645/0022-3395(2000)086[0537:irsogs]2.0.co;2

Almeyda-Artigas, R. J., Bargues, M. D. y Mas-Coma, S. (2000b). rDNA of Gnathostoma species (Nematoda): ITS-2 microsatellites and 5.8 S gene secondary structure. Research and Reviews in Parasitology, 60, 51–56.

Almeyda-Artigas, R. J., Mosqueda-Cabrera, M. Á. y Sánchez-Núñez, E. (2010). Precocity of Gnathostoma turgidum in naturally infected four-eyed opossum Philander opossum pallidus from Temascal, Oaxaca, Mexico. Parasitology Research, 106, 439–443. https://doi.org/10.1007/s00436-009-1682-8

Álvarez-Guerrero, C. y Alba-Hurtado, F. (2007). Estuarine fish and turtles as intermediate and paratenic hosts of Gnathostoma binucleatum in Nayarit, Mexico. Parasitology Research, 102, 117–122. https://doi.org/10.1007/s00436-007-0738-x

Bertoni-Ruiz, F., García-Prieto, L., Osorio-Sarabia, D. y León-Règagnon, V. (2005). A new species of Gnathostoma (Nematoda: Gnathostomatidae), parasite of Procyon lotor hernandezii from Mexico. Journal of Parasitology, 91, 1143–1149. https://doi.org/10.1645/ge-516r.1

Bush, A. O., Lafferty, K. D., Lotz, J. M. y Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, 83, 575–583.

Cole, R. A., Choudhury, A., Nico, L. G. y Griffin, K. M. (2014). Gnathostoma spinigerum in live Asian swamp eels (Monopterus spp.) from food markets and wild populations, United States. Emerging Infectious Diseases, 20, 634–642. https://doi.org/10.3201/eid2004.131566

Conagua (Comisión Nacional del Agua). (2021). Programa Hídrico Regional 2021-2024. Región Hidrológico-Administrativa XI Frontera Sur. Ciudad de México: Secretaría de Medio Ambiente y Recursos Naturales, Comisión Nacional del Agua.

Dias, C. A. y Perini, F. A. (2018). Biogeography and early emergence of the genus Didelphis (Didelphimorphia, Mammalia). Zoologica Scripta, 47, 645–654.

Díaz-Camacho, S. P., Delgado-Vargas, F., Willms, K., de la Cruz-Otero, M. C., Rendón-Maldonado, J. G., Robert, L. et al. (2010). Intrahepatic growth and maturation of Gnathostoma turgidum in the natural definitive opossum host, Didelphis virginiana. Parasitology International, 59, 338–343. https://doi.org/10.1016/j.parint.2010.04.004

García-Márquez, L. J., Lamothe-Argumedo, R., Osorio-Sarabia, D., García-Prieto, L. y León-Règagnon, V. (2009). Morphological and molecular identification of Gnathostoma binucleatum (Nematoda: Gnathostomatidae) advanced third stage larvae (AdvL3) in the state of Colima, Mexico. Revista Mexicana de Biodiversidad, 80, 867–870. https://doi.org/10.22201/ib.20078706e.2009.003.157

Gardner, A. L. (1973). The systematics of the genus Didelphis (Marsupialia: Didelphidae) in North and Middle America. Special Publications of the Museum Texas Tech University, 4, 1–81.

Gaspar-Navarro, J., Almeyda-Artigas, R. J., Sánchez-Miranda, E., Carranza-Calderón, L. y Mosqueda-Cabrera, M. A. (2013). Description of advanced third-stage larvae of Gnathostoma lamothei Bertoni-Ruiz et al. 2005 (Nematoda: Gnathostomatidae) from experimental hosts and contributions to its life cycle. Parasitology Research, 112, 169–175. https://doi.org/10.1007/s00436-012-3122-4

Hebert, P. D., Cywinska, A., Ball, S. L. y DeWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270, 313–321. https://doi.org/10.1098/rspb.2002.2218

Hernández-Gómez, R. E., Martínez-Salazar, E. A., López-Jiménez, S. y León-Règagnon, V. (2010). Molecular identification of the advanced third-stage larvae (AdvL3) of Gnathostoma lamothei in Tabasco, Mexico. Parasitology International, 59, 97-99. https://doi.org/10.1016/j.parint.2009.10.008

Maddison, W. P. y Maddison, D. R. (2019). Mesquite: a modular system for evolutionary analysis, version 3.6. 2018.

Messing, J. (1993). M13 cloning vehicles. Their contribution to DNA sequencing. Methods in Molecular Biology, 23, 9–22. https://doi.org/10.1385/0-89603-248-5:9

Miyazaki, I. (1954). Studies on Gnathostoma ocurring in Japan (Nematoda: Gnathostomidae). II. Life history of Gnathostoma and morphological comparison of its larval forms. Kyushu Memoirs of Medical Science, 5, 123–39.

Mosqueda-Cabrera, M. Á., Sánchez-Miranda, E., Carranza-Calderón, L. y Ortiz-Nájera, H. E. (2009). Finding advanced third-stage larvae of Gnathostoma turgidum Stossich, 1902 in Mexico from natural and experimental host and contributions to the life cycle description. Parasitology Research, 104, 1219–1225. https://doi.org/10.1007/s00436-008-1318-4

Mosqueda-Cabrera, M. Á., Desentis-Pérez, D. L., Padilla-Bejarano, T. A. y García-Prieto, L. (2023). Possible zoonotic implications of the discovery of the advanced third stage larva of Gnathostoma turgidum (Spirurida: Gnathostomatidae) in a Mexican fish species. Helminthologia, 60, 112–116. https://doi.org/10.2478/helm-2023-0011

Pérez-Álvarez, Y., García-Prieto, L., Osorio-Sarabia, D., Lamothe-Argumedo, R. y León-Règanon, V. (2008). Present distribution of the genus Gnathostoma (Nematoda: Gnathostomatidae) in México. Zootaxa, 1930, 39–55. https://doi.org/10.11646/zootaxa.1930.1.3

Prosser, S. W., Velarde‐Aguilar, M. G., León‐Règagnon, V. y Hebert, P. D. (2013). Advancing nematode barcoding: a primer cocktail for the cytochrome c oxidase subunit I gene from vertebrate parasitic nematodes. Molecular Ecology Resources, 13, 1108–1115. https://doi.org/10.1111/1755-0998.12082

Rambaut, A. (2006). Figtree. Tree figure drawing tool. Version 1.4. 2. Institute of Evolutionary Biology.

Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S. et al. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys029

Published

2025-02-06

How to Cite

Mosqueda-Cabrera, M. Ángel, Desentis-Pérez, D. L. ., & Padilla-Bejarano, T. A. . (2025). The high morphological variation found in the immature stages of the nematode Gnathostoma sp. I is not supported by molecular information. Revista Mexicana De Biodiversidad, 96, e965098. https://doi.org/10.22201/ib.20078706e.2025.96.5098

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Section

TAXONOMÍA Y SISTEMÁTICA