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Phylogeny, species delimitation and ecological and morphological diversity of Characithecium (Monogenoidea: Dactylogyridae)

Published online by Cambridge University Press:  03 March 2022

Emília W. Wendt Open the ORCID record for Emília W. Wendt [Opens in a new window] ,
Luiz R. Malabarba ,
Mariana P. Braga Open the ORCID record for Mariana P. Braga [Opens in a new window] ,
Walter A. Boeger ,
Michael Landis  and
Tiago P. Carvalho
Emília W. Wendt*
Affiliation:
Laboratório de Ictiologia, Departamento de Zoologia, Universidade Federal do Rio Grande do Sul – UFRGS, Av. Bento Gonçalves, 9500, Bloco 4, prédio 43435, 91501-970 Porto Alegre, RS, Brazil
Luiz R. Malabarba
Affiliation:
Laboratório de Ictiologia, Departamento de Zoologia, Universidade Federal do Rio Grande do Sul – UFRGS, Av. Bento Gonçalves, 9500, Bloco 4, prédio 43435, 91501-970 Porto Alegre, RS, Brazil
Mariana P. Braga
Affiliation:
Department of Biology, Washington University in St. Louis, St. Louis, MO 63130, USA
Walter A. Boeger
Affiliation:
Biological Interactions and Departamento de Zoologia, Centro Politécnico, Setor de Ciências Biológicas, Universidade Federal do Paraná (UFPR), Caixa Postal 19073, CEP 81531-980, Curitiba, Paraná, Brazil
Michael Landis
Affiliation:
Department of Biology, Washington University in St. Louis, St. Louis, MO 63130, USA
Tiago P. Carvalho
Affiliation:
Laboratório de Ictiologia, Departamento de Zoologia, Universidade Federal do Rio Grande do Sul – UFRGS, Av. Bento Gonçalves, 9500, Bloco 4, prédio 43435, 91501-970 Porto Alegre, RS, Brazil Laboratorio de Ictiología, Unidad de Ecología y Sistemática (UNESIS), Departamento de Biología, Facultad de Ciencias, Pontificia Universidad Javeriana, Carrera 7 No. 43-82, Bogotá D.C., Colombia
*
Author for correspondence: Emília W. Wendt, E-mail: [email protected]
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Abstract

Characithecium (Monogenoidea, Dactylogyridae) is a genus containing nine species that live on the gills of a characid clade containing genera Astyanax, Andromakhe, Psalidodon and Oligosarcus (Characiformes, Characidae) in South and Central America. Earlier studies suggest a tight coevolutionary history between these parasites and their hosts mainly due to the phylogenetic proximity between these genera of fish. Hence, this study explores phylogenetic relationships, species limits and extrinsic factors (geography and ecology) explaining parasite prevalence. To understand the evolutionary history of the genus, we constructed a time-calibrated phylogenetic hypothesis, which includes eight of the nine known species of Characithecium sampled from a broad spectrum of host species. The phylogeny supports the monophyly of Characithecium, with its most recent common ancestor dating from the Miocene. Using generalized mixed-yule coalescent and Bayesian Poisson tree process methods, species delimitation analyses suggested fewer species than the proposed delimitation based on morphology alone, recovering four and six entities, respectively. The results indicate that species of Characithecium have wider geographical and host distribution and higher prevalence on Oligosarcus species compared to Astyanax and Psalidodon. Correlation between parasite prevalence and biotic and abiotic traits, based on generalized linear models, indicates that the frequency of occurrence of different species of Characithecium is associated with distinct factors, such as host genus, high altitudes, rivers and streams, and different ecoregions. Our results suggest that species of Characithecium are highly opportunistic, exploring resources in different manner as our data reveal the ability of these parasites to explore a diverse environment of variable biotic (e.g. hosts) and abiotic features.

Keywords

Divergence time estimateshost–parasite associationsmolecular phylogenymorphologicaltaxonomy
Type
Research Article
Information
Parasitology , Volume 149 , Issue 5 , April 2022 , pp. 700 - 716
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Abell, R, Thieme, ML, Revenga, C, Bryer, M, Kottelat, M, Bogutskaya, N, Coad, B, Mandrak, N, Balderas, SC, Bussing, W, Stiassny, MLJ, Skelton, P, Allen, GR, Unmack, P, Naseka, A, Ng, R, Sindorf, N, Robertson, J, Armijo, E, Higgins, JV, Heibel, TJ, Wikramanayake, E, Olson, D, López, HL, Reis, RE, Lundberg, JG, Sabaj, MH and Petry, P (2008) Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. BioScience 58, 403–414.CrossRefGoogle Scholar
Agosta, SJ and Brooks, DR (2020) The Major Metaphors of Evolution: Darwinism Then and Now. Evolutionary Biology – New Perspectives on Its Development. Cham: Springer International Publishing.CrossRefGoogle Scholar
Agosta, SJ and Klemens, JA (2008) Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecology Letters 11, 1123–1134.CrossRefGoogle ScholarPubMed
Agosta, SJ, Janz, N and Brooks, DR (2010) How specialists can be generalists: resolving the ‘parasite paradox’ and implications for emerging infectious disease. Zoologia 27, 151–162.CrossRefGoogle Scholar
Albert, JS, Tagliacollo, VA and Dagosta, F (2020) Diversification of Neotropical freshwater fishes. Annual Review of Ecology, Evolution, and Systematics 51, 27–53.CrossRefGoogle Scholar
Araujo, SB, Braga, MP, Brooks, DR, Agosta, SJ, Hoberg, EP, von Hartenthal, FW and Boeger, WA (2015) Understanding host-switching by ecological fitting. PLoS One 10, 1–17.CrossRefGoogle ScholarPubMed
Benovics, M, Desdevises, Y, Šanda, R, Vukić, J, Scheifler, M, Doadrio, I, Sousa-Santos, C and Šimková, A (2020) High diversity of fish ectoparasitic monogeneans (Dactylogyrus) in the Iberian Peninsula: a case of adaptive radiation? Parasitology 147, 418–430.CrossRefGoogle ScholarPubMed
Boeger, WA and Vianna, RT (2006) Monogenoidea, in Amazon fish parasites. In Thatcher, VE (ed.), Amazon Fish Parasites. Bulgaria: Pensoft, pp. 42–116.Google Scholar
Bouckaert, R, Heled, J, Kühnert, D, Vaughan, T, Wu, CH, Xie, D, Suchard, MA, Rambaut, A and Drummond, AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.CrossRefGoogle ScholarPubMed
Braga, MP, Razzolini, E and Boeger, WA (2015) Drivers of parasite sharing among Neotropical freshwater fishes. Journal of Animal Ecology 84, 487–497.CrossRefGoogle ScholarPubMed
Brooks, DR and Agosta, SJ (2012) Children of time: the extended synthesis and Major metaphors of evolution. Zoologia 29, 497–514.CrossRefGoogle Scholar
Brooks, DR and McLennan, DA (2002) The Nature of Diversity: An Evolutionary Voyage of Discovery, 2nd Edn. Chicago, USA: University of Chicago Press.CrossRefGoogle Scholar
Brooks, DR, Hoberg, EP, Boeger, WA, Gardner, SL, Galbreath, KE, Herczeg, D, Mejía-Madrid, HH, Rácz, SE and Dursahinhan, AT (2014) Finding them before they find us: informatics, parasites, and environments in accelerating climate change. Comparative Parasitology 81, 155–164.CrossRefGoogle Scholar
Brooks, DR, Hoberg, EP and Boeger, WA (2019) The Stockholm Paradigm: Climate Change and Emerging Disease, 1st Edn. Chicago: University of Chicago Press.Google Scholar
Bueno-Silva, M (2012) Genética molecular e sistemática animal: um breve histórico, contribuições e desafios. Estudos de Biologia 34, 157–163.CrossRefGoogle Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Multimodel Inference: A Practical Information and Theoretic Approach, 2nd Edn. New York: Springer.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on terms: Margolis et al. revisited. The Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Cohen, SC, Justo, MC and Kohn, A (2013) South American Monogenoidea Parasites of Fishes, Amphibians and Reptiles. Rio de Janeiro: Oficina de Livros.Google Scholar
Costa-Pereira, R, Araújo, MS, Paiva, F and Tavares, LER (2016) Functional morphology of the tetra fish Astyanax lacustris differs between divergent habitats in the Pantanal wetlands. Journal of Fish Biology 89, 1450–1458.CrossRefGoogle ScholarPubMed
da Graca, RJ, Fabrin, TMC, Gasques, LS, Prioli, SMAP, Balbuena, JA, Prioli, AJ and Takemoto, RM (2018) Topological congruence between phylogenies of Anacanthorus spp. (Monogenea: Dactylogyridae) and their Characiformes (Actinopterygii) hosts: a case of host–parasite cospeciation. PLoS One 13, e0193408.CrossRefGoogle ScholarPubMed
da Silva, BAF, da Silva, RJ and Yamada, FH (2021) Characithecium spp. (Monogenea: Dactylogyridae) from Astyanax bimaculatus (Characiformes: Characidae) in Northeast Brazil, with description of a new species. Acta Parasitology 66, 1307–1315.CrossRefGoogle ScholarPubMed
Domingues, MV and Boeger, WA (2005) Neotropical Monogenoidea. 47. Phylogeny and coevolution of species of Rhinoxenus (Platyhelminthes, Monogenoidea, Dactylogyridae) and their Characiformes hosts (Teleostei, Ostariophysi) with description of four new species. Zoosystema 27, 441–467.Google Scholar
Ezard, T, Fujisawa, T and Barraclough, TG (2009) SPLITS: SPecies’ LImits by Threshold Statistics. R package version 1.0-18/r45. Available at http://R-Forge.R-project.org/projects/splits/ (accessed 15 January 2020).Google Scholar
Fujisawa, T and Barraclough, TG (2013) Delimiting species using single-locus data and the generalized mixed yule coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62, 707–724.CrossRefGoogle ScholarPubMed
Gallas, M, Calegaro-Marques, C and Amato, SB (2016) A new species of Characithecium (Monogenea: Dactylogyridae) from external surface and gills of two species of Astyanax (Ostariophysi: Characidae) in southern Brazil. Revista Mexicana de Biodiversidad 87, 903–907.CrossRefGoogle Scholar
Gioia, I, Cordeiro, NS and Artigas, PT (1988) Urocleidoides astyanacis n. sp. (Monogenea: Ancyrocephalinae) from freshwater characidians of the genus Astyanax. Memórias do Instituto Oswaldo Cruz 83, 13–15.CrossRefGoogle Scholar
Heled, J and Drummond, AJ (2010) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27, 570–580.CrossRefGoogle ScholarPubMed
Hoberg, EP and Brooks, DR (2015) Evolution in action: climate change, biodiversity dynamics and emerging infectious disease. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 370, 20130553.CrossRefGoogle ScholarPubMed
Humason, GL (1979) Animal Tissue Techniques, 4th Edn. San Francisco: WH Freeman and Co.Google Scholar
Huyse, T and Volckaert, FAM (2005) Comparing host and parasite phylogenies: Gyrodactylus flatworms jumping from goby to goby. Systematic Biology 54, 710–718.CrossRefGoogle ScholarPubMed
Janzen, DH (1985) On ecological fitting. Oikos 45, 308–310.CrossRefGoogle Scholar
Katoh, K, Misawa, K, Kuma, KI and Miyata, K (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.CrossRefGoogle ScholarPubMed
Kearn, GC (1994) Evolutionary expansion of the Monogenea. International Journal for Parasitology 24, 1227–1271.CrossRefGoogle ScholarPubMed
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Mentjies, P and Drummond, A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 1647–1649.CrossRefGoogle ScholarPubMed
Kritsky, DC and Leiby, PD (1972) Dactylogyridae (Monogenea) from the freshwater fish, Astyanax fasciatus (Cuvier), in Costa Rica, with descriptions of Jainus hexops sp. n., Urocleidoides costaricensis, and U. heteroancistrium combs. n. Proceedings of the Helminthological Society of Washington 39, 227–230.Google Scholar
Lanfear, R, Calcott, B, Ho, SYW and Guindon, S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.CrossRefGoogle ScholarPubMed
Lemey, P, Salemi, M and Vandamme, AM (2009) The Phylogenetic Handbook: A Practical Approach to Phylogenetic Analysis and Hypothesis Testing. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Littlewood, DTJ and Olson, PD (2001) Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In Littlewood, DTJ and Bray, RA (eds), Interrelationships of the Platyhelminthes. New York: Taylor and Francis Publishing, pp. 262–278.Google Scholar
Lucena, CAS, Calegari, BB, Pereira, EHL and Dallegrave, E (2013) O uso de óleo de cravo na eutanásia de peixes. Boletim Sociedade Brasileira de Ictiologia 105, 20–24.Google Scholar
Mendlová, M and Šimková, A (2014) Evolution of host specificity in monogeneans parasitizing African cichlid fish. Parasites & Vectors 7, 69.CrossRefGoogle ScholarPubMed
Mendoza-Franco, EF, Reina, RG and Torchin, ME (2009) Dactylogyrids (Monogenoidea) parasitizing the gills of Astyanax spp. (Characidae) from Panama and Southeast Mexico, a new species of Diaphorocleidus and a proposal for Characithecium N. Gen. Journal of Parasitology 95, 46–55.CrossRefGoogle Scholar
Mendoza-Palmero, CA, Rossin, MA, Irigoitia, MM and Scholz, T (2020) A new species of Ameloblastella Kritsky, Mendoza-Franco & Scholz, 2000 (Monogenoidea: Dactylogyridae) from South American freshwater catfishes (Siluriformes: Pimelodidae). Systematic Parasitology 97, 357–367.CrossRefGoogle Scholar
Miller, M, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, LA.CrossRefGoogle Scholar
Mirande, JM (2020) Morphology, molecules and the phylogeny of Characidae (Teleostei, Characiformes). Cladistics 35, 282–300.CrossRefGoogle Scholar
Mollaret, I, Lim, LH and Justine, J (2000) Phylogenetic position of the monogeneans Sundanonchus, Thaparocleidus, and Cichlidogyrus inferred from 28S rDNA sequences. International Journal for Parasitology 30, 659–662.CrossRefGoogle ScholarPubMed
Nee, S, May, RM and Harvey, PH (1994) The reconstructed evolutionary process. Philosophical Transactions of the Royal Society of London B: Biological Sciences 344, 305–311.Google ScholarPubMed
Ondračková, M, Seifertová, M, Bryjová, A, Leis, E and Jurajda, P (2020) Morphometric and genetic evidence for cryptic diversity in Gyrodactylus (Monogenea) infecting non-native European populations of Ameiurus nebulosus and A. melas. Parasitology 147, 1700–1711.CrossRefGoogle ScholarPubMed
Patella, L, Brooks, DR and Boeger, WA (2017) Phylogeny and ecology illuminate the evolution of associations under the Stockholm paradigm: Aglaiogyrodactylus spp. (Platyhelminthes, Monogenoidea, Gyrodactylidae) and species of Loricariidae (Actinopterygii, Siluriformes). Vie et Milieu 67, 91–102.Google Scholar
Penn, O, Privman, E, Ashkenazy, H, Landan, G, Graur, D and Pupko, T (2010) GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Research 38, 23–28.CrossRefGoogle ScholarPubMed
Pinacho-Pinacho, CD, Calixto-Rojas, M, García-Vásquez, A, Guzmán-Valdivieso, I, Barrios-Gutiérrez, JJ and Rubio-Godoy, M (2021) Species delimitation of Gyrodactylus (Monogenea: Gyrodactylidae) infecting the southernmost cyprinids (Actinopterygii: Cyprinidae) in the New World. Parasitology Research 120, 831–848.CrossRefGoogle ScholarPubMed
Pons, J, Barraclough, T, Gomez-Zurita, J, Cardoso, A, Duran, D, Hazell, S, Kamoun, S, Sumlin, W and Vogler, A (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.CrossRefGoogle ScholarPubMed
Poulin, R (1992) Determinants of host-specificity in parasites of fresh-water fishes. International Journal for Parasitology 22, 753–758.CrossRefGoogle Scholar
Poulin, R and Justine, JL (2008) Linking species abundance distributions and body size in monogenean communities. Parasitology Research 103, 187–193.CrossRefGoogle ScholarPubMed
Poulin, R, Blanar, CA, Thieltges, DW and Marcogliese, DJ (2011 a) The biogeography of parasitism in sticklebacks: distance, habitat differences and the similarity in parasite occurrence and abundance. Ecography 34, 540–551.CrossRefGoogle Scholar
Poulin, R, Krasnov, BR and Mouillot, D (2011 b) Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.CrossRefGoogle ScholarPubMed
Qing, X, Bert, W, Gamliel, A, Bucki, P, Duvrinin, S, Alon, T and Miyara, SB (2019) Phylogeography and molecular species delimitation of Pratylenchus capsici N. sp., a new root-lesion nematode in Israel on pepper (Capsicum annuum). Phytopathology 109, 847–858.CrossRefGoogle Scholar
Rambaut, A, Suchard, MA, Xie, D and Drummond, AJ (2014) Tracer v1.6. Available at http://beast.bio.ed.ac.uk/Tracer (accessed 29 August 2019).Google Scholar
Ribeiro, AC (2006) Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of eastern Brazil: an example of faunal evolution associated with a divergent continental margin. Neotropical Ichthyology 4, 225–246.CrossRefGoogle Scholar
Ribeiro, AC and Menezes, NA (2015) Phylogenetic relationships of the species and biogeography of the characid genus Oligosarcus Günther, 1864 (Ostariophysi, Characiformes, Characidae). Zootaxa 3949, 41–81.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MRBAYES 3.2: efficient Bayesian phylogenetic inference and model selection across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle Scholar
Rossin, MA and Timi, JT (2015) Characithecium (Monogenoidea: Dactylogyridae) parasitic on the Neotropical fish Oligosarcus jenynsii (Teleostei: Characidae) from the Pampasic region, Argentina, with the emendation of the genus. Zootaxa 3893, 382–396.CrossRefGoogle Scholar
Ruttkay, H, Solignac, M and Sperlich, D (1992) Nuclear and mitochondrial ribosomal RNA variability in the obscura group of Drosophila. Genetica 85, 143–179.CrossRefGoogle ScholarPubMed
Scarpa, F, Cossu, P, Sanna, D, Lai, T, Norenburg, JL, Curini-Galletti, M and Casu, M (2015) An 18S rDNA and 28S rDNA-based clock calibration for marine Proseriata (Platyhelminthes). Journal of Experimental Marine Biology and Ecology 463, 22–31.CrossRefGoogle Scholar
Tamura, K and Nei, M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google ScholarPubMed
Terán, GE, Benitez, MF and Mirande, JM (2020) Opening the Trojan horse: phylogeny of Astyanax, two new genera and resurrection of Psalidodon (Teleostei: Characidae). Zoological Journal of the Linnean Society 190, 1217–1234.Google Scholar
Tkach, V and Pawlowski, J (1999) A new method of DNA extraction from the ethanol-fixed parasitic worms. Acta Parasitologica 44, 147–148.Google Scholar
Untergasser, A, Nijveen, H, Rao, X, Bisseling, T, Geurts, R and Leunissen, JA (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research 35, 71–74.CrossRefGoogle ScholarPubMed
Vanhove, MPM, Tessens, B, Schoelinck, C, Jondelius, U, Littlewood, DTJ, Artois, T and Huyse, T (2013) Problematic barcoding in flatworms: a case-study on monogeneans and rhabdocoels (Platyhelminthes). ZooKeys 365, 355–379.CrossRefGoogle Scholar
Wendt, EW, Silva, PC, Malabarba, LR and Carvalho, TP (2019) Phylogenetic relationships and historical biogeography of Oligosarcus (Teleostei: Characidae): examining riverine landscape evolution in southeastern South America. Molecular Phylogenetics and Evolution 140, 106604.CrossRefGoogle ScholarPubMed
Zago, AC, Franceschini, L, Abdallah, VD, Müller, MI, Azevedo, RK and da Silva, RJ (2021) Morphological and molecular data of new species of Characithecium and Diaphorocleidus (Monogenea: Dactylogyridae) from Neotropical characid fishes. Parasitology International 88, 102406.CrossRefGoogle Scholar
Zhang, J, Kapli, P, Pavlidis, P and Stamatakis, A (2013) A general Species delimitation method with applications to phylogenetic placements. Bioinformatics (Oxford, England) 29, 2869–2876.CrossRefGoogle ScholarPubMed
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