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Host-induced phenotypic plasticity in Saccocoelioides lamothei Aguirre-Macedo and Violante-González, 2008 (Digenea: Haploporidae) a parasite of freshwater, brackish and marine fishes from Middle America

Published online by Cambridge University Press:  10 December 2020

Marcelo Tonatiuh González-García ,
Leopoldo Andrade-Gómez ,
Carlos Daniel Pinacho-Pinacho ,
Ana Lucia Sereno-Uribe  and
Martín García-Varela Open the ORCID record for Martín García-Varela [Opens in a new window]
Marcelo Tonatiuh González-García
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Ciudad de México, México
Leopoldo Andrade-Gómez
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Ciudad de México, México Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C. P. 04510, Ciudad de México, México
Carlos Daniel Pinacho-Pinacho
Affiliation:
Investigador Cátedras CONACyT, Instituto de Ecología, A.C., Red de Estudios Moleculares Avanzados, Km 2.5 Ant. Carretera a Coatepec, Xalapa, Veracruz91070, México
Ana Lucia Sereno-Uribe
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Ciudad de México, México
Martín García-Varela*
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Avenida Universidad 3000, Ciudad Universitaria, C.P. 04510, Ciudad de México, México
*
Author for correspondence: Martín García-Varela, E-mail: [email protected]
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Abstract

Saccocoelioides is a genus of trematodes associated with fishes from the Americas. In the current research, morphologically distinct specimens of Saccocoelioides spp. were collected from six countries in Middle America. Specimens were sequenced using three molecular markers, the domains D1–D3 of the large subunit (LSU) from the nuclear rDNA, the cytochrome c oxidase subunit 1 (cox1) and nicotinamide adenine dinucleotide dehydrogenase subunit 1 (nad1) from mitochondrial DNA. A total of 74 new sequences were compared and aligned with other sequences available in GenBank. Maximum likelihood and Bayesian inference analyses were inferred from the LSU and cox1 datasets, revealing unequivocally that all the specimens correspond to S. lamothei. A haplotype network was built with 119 sequences of the nad1 gene. The network detected 57 distinct haplotypes divided into three haplogroups. To explore morphological differences among samples of S. lamothei, 17 morphological features were measured from 53 specimens from three fish families: Eleotridae, Mugilidae and Gobiidae. Principal component analysis yielded three main polygons that corresponded with each family analysed, suggesting host-induced phenotypic plasticity. The current evidence suggests that S. lamothei infects at least five fish families along the Pacific coasts of Mexico, Guatemala, El Salvador, Honduras, Nicaragua and Costa Rica.

Keywords

Definitive hostsmolecular markersphenotypic plasticitytaxonomyTrematoda
Type
Research Article
Information
Parasitology , Volume 148 , Issue 5 , April 2021 , pp. 519 - 531
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Aguirre-Macedo, ML and Violante-González, J (2008) Saccocoelioides lamothei N. sp. from Dormitator latifrons (Pisces: Eleotridae) from coastal lagoons of Guerrero, Mexico. Revista Mexicana de Biodiversidad 79, 33–40.Google Scholar
Andrade-Gómez, L, Pinacho-Pinacho, CD, Hernández-Orts, JS, Sereno-Uribe, AL and García-Varela, M (2016) Morphological and molecular analyses of a new species of Saccocoelioides Szidat, 1954 (Haploporidae Nicoll, 1914) in the fat sleeper Dormitator maculatus (Bloch) (Perciformes: Eleotridae) from the Gulf of Mexico. Journal of Helminthology 26, 1–13.Google Scholar
Andrade-Gómez, L, Pinacho-Pinacho, CD and García-Varela, M (2017) Molecular, morphological and ecological data of Saccocoelioides Szidat, 1954 (Digenea: Haploporidae) from Middle America supported the reallocation from Culuwiya cichlidorum to Saccocoelioides. Journal of Parasitology 103, 257–267.CrossRefGoogle ScholarPubMed
Andrade-Gómez, L, Sereno-Uribe, AL and García-Varela, M (2019) Description of a new species and understanding the genetic diversity of Saccocoelioides Szidat, 1954 (Haploporidae) in Middle America using mitochondrial and nuclear DNA sequences. Parasitology International 71, 87–98.CrossRefGoogle ScholarPubMed
Andres, MJ, Pulis, EE, Curran, SS and Overstreet, RM (2018) On the systematics of some marine haploporids (Trematoda) with the description of a new species of Megasolena Linton, 1910. Parasitology International 67, 805–815.CrossRefGoogle ScholarPubMed
Bandelt, H, Forster, JP and Röhl, A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Blankespoor, HD (1974) Host induced variation in Plagiorchis noblei Park, 1936 (Plagiorchiidae: Trematoda). American Midland Naturalist 92, 415–433.CrossRefGoogle Scholar
Blasco-Costa, I, Balbuena, JA, Raga, JA, Kostadinova, A and Olson, PD (2010) Molecules and morphology reveal cryptic variation among digeneans infecting sympatric mullets in the Mediterranean. Parasitology 137, 287–302.CrossRefGoogle ScholarPubMed
Colín, A, Hernández-Pérez, Z, Guevara-Chumacero, LM, Castañeda-Rico, S, Serrato-Díaz, A and Ibáñez, AL (2020) Are striped mullet (Mugil cephalus) philopatric? Marine Biology 167, 10.CrossRefGoogle Scholar
Curran, SS, Pulis, EE, Andres, MJ and Overstreet, RM (2018) Two new species of Saccocoelioides (Digenea: Haploporidae) with phylogenetic analysis of the family, including species of Saccocoelioides from North, Middle and South America. Journal of Parasitology 104, 221–239.CrossRefGoogle ScholarPubMed
Dayrat, B (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society 85, 407–415.CrossRefGoogle Scholar
De Silva, SS (1980) Biology of juvenile grey mullet: a short review. Aquaculture 19, 21–36.CrossRefGoogle Scholar
Díaz, MT and González, GT (1990) Ciclo de vida de Saccocoelioides tarpazensis n. sp. (Trematoda: Haploporidae). Parasitologia 41, 327–336.Google Scholar
Díaz, MT, Bashirullah, AK, Hernández, LE and Gómez, E (2009) Life cycle of Culuwiya tilapiae (Nasir y Gómez1976) (Trematoda: Haploporidae) in Venezuela. Revista Científica 5, 439–445.Google Scholar
Funicelli, NA, Meineke, DA, Bryant, HE, Dewey, MR, Ludwig, GM and Mengel, LS (1989) Movements of striped mullet, Mugil cephalus, tagged in Everglades National Park. Florida Bulletin of Marine Science 44, 171–178.Google Scholar
Gallas, M and Utz, LRP (2019) Revalidation of Saccocoelioides bacilliformis (Digenea, Haploporidae) parasitizing species of Astyanax (Characiformes, Characidae) from southern Brazil. Iheringia Série Zoologia 109, e2019039.CrossRefGoogle Scholar
Galvan-Quesada, S, Doadrio, I, Alda, F, Perdices, A, Reina, RG, Garcia Varela, M, Hernandez, N, Campos Mendoza, A, Bermingham, E and Dominguez-Dominguez, O (2016) Molecular phylogeny and biogeography of the amphidromous fish genus Dormitator Gill 1861 (Teleostei: Eleotridae). PLoS ONE 11, e0153538. doi: 10.1371/journal.pone.0153538CrossRefGoogle Scholar
García-Varela, M and Nadler, SA (2005) Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rRNA gene sequences. Journal of Parasitology 91, 1401–1409.CrossRefGoogle Scholar
Gouy, M, Guindon, S and Gascuel, O (2010) Seaview version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221–224.CrossRefGoogle ScholarPubMed
Hildebrand, J, Adamcyk, M, Laskowski, Z and Zaleśny, G (2015) Host-dependent morphology of Isthmiophora melis (Schrank, 1788) Luhe, 1909 (Digenea, Echinostomatinae) morphological variation vs molecular stability. Parasites & Vectors 8, 481.CrossRefGoogle ScholarPubMed
Ibáñez, AL, Chang, CW, Hsu, CC, Wang, CH, Iizuka, Y and Tzeng, WN (2012) Diversity of migratory environmental history of the mullets Mugil cephalus and M. curema in Mexican coastal waters as indicated by otolith Sr: Ca ratios. Ciencias Marinas 38, 73–87.CrossRefGoogle Scholar
Kostadinova, A, Herniou, EA, Barrett, J and Littlewood, DTJ (2003) Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA And morphological analyses. Systematic Parasitology 54, 159–176.CrossRefGoogle ScholarPubMed
Maddison, WP and Maddison, DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.7.5. Available at http://mesquiteproject.org/.Google Scholar
Martorelli, SR (1986) Estudios parasitologicos en biotipos lenticos de la República Argentina III. El ciclo biológico de Saccocoelioides carolae Lunaschi (Digenea) parásitos de Cichlasoma facetum (Jenyns, 1842) (Pisces: Cichlidae). Neotropical 88, 125–132.Google Scholar
Miller, RR, Minckley, WL and Norris, SM (2005) Freshwater Fishes of Mexico Chicago. Illinois: The University of Chicago Press.Google Scholar
Miller, AM, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE), 1–8. doi: 10.1109/GCE.2010.5676129Google Scholar
Miner, BG, Sultan, SE, Morgan, SG, Padilla, DK and Relyea, RA (2005) Ecological consequences of phenotypic plasticity. Trends in Ecology & Evolution 20, 685–692.CrossRefGoogle ScholarPubMed
Morgan, JAT and Blair, D (1998) Mitochondrial ND1 gene sequences used to identify echinostome isolates from Australia and New Zealand. International Journal for Parasitology 28, 493–502.CrossRefGoogle ScholarPubMed
Nadler, SA, D´Amelio, S, Fagerholm, HP, Berland, B and Paggi, L (2000) Phylogenetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Høst, 1932 (Nematoda: Ascaridoidea) based on nuclear rDNA sequence data. Parasitology 121, 455–463.CrossRefGoogle ScholarPubMed
Nirchio, M, Oliveira, C, Siccha-Ramirez, ZR, de Sene, VF, Sola, L, Milana, V and Rossi, AR (2017) The Mugil curema species complex (Pisces, Mugilidae): a new karyotype for the Pacific white mullet mitochondrial lineage. Comparative Cytogenetic 11, 225–237.CrossRefGoogle ScholarPubMed
Pérez-Ponce de León, G (1995) Host-induced morphological variability in adult Posthodiplostomum minimum (Digenea: Neodiplostomidae). Journal of Parasitology 81, 818–820.CrossRefGoogle Scholar
Pérez-Ponce de León, G and Nadler, SA (2011) Integrating molecular and morphological approaches for characterization parasites cryptic species: implications for parasitology. Parasitology 138, 1688–1709.Google Scholar
Pinacho-Pinacho, CD, García-Varela, M, Hernández-Orts, JS, Mendoza-Palmero, CA, Sereno-Uribe, AL, Martínez-Ramírez, E, Andrade-Gómez, L, Hernández-Cruz, E, López-Jiménez, CA and Pérez-Ponce de León, G (2015) Checklist of the helminth parasites of genus Profundulus Hubbs, 1924 (Cyprinodontiformes: Profundulidae), an endemic family of freshwater fishes in Middle-America. Zookeys 523, 1–30.CrossRefGoogle Scholar
Posada, D (2008) Jmodeltest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Poulin, R (2007) Evolutionary Ecology of Parasites, 2nd Edn. Princeton: Princeton University Press.CrossRefGoogle Scholar
Poulin, R (2011) Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biology Letters 7, 241–244.CrossRefGoogle ScholarPubMed
Poulin, R and Presswell, B (2016) Taxonomic quality of species descriptions varies over time and with the number of authors, but unevenly among parasitic taxa. Systematic Biology 65, 1107–1116.CrossRefGoogle ScholarPubMed
Rambaut, A (2012) FigTree v1.4.0. Institute of Evolutionary Biology. University of Edinburgh, UK.Google Scholar
R Core Team (2016) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Core Team. Available at https://www.R-project.org/.Google Scholar
Ronquist, F, Teslenko, M, Van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, M and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Silvestro, D and Michalak, I (2011) RaxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution 12, 335–337.CrossRefGoogle Scholar
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Thomson, JM (1997) The Mugilidae of the world. Memoirs of the Queensland Museum 41, 457–562.Google Scholar
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