Integrative taxonomy reveals an even greater diversity within the speciose genus Phyllodistomum (Platyhelminthes : Trematoda : Gorgoderidae), parasitic in the urinary bladder of Middle American freshwater fishes, with descriptions of five new species
Carlos D. Pinacho-Pinacho
A , Ana L. Sereno-Uribe B , Jesús S. Hernández-Orts C , Martín García-Varela B and Gerardo Pérez-Ponce de León B D E
+ Author Affiliations
- Author Affiliations
A Cátedras CONACyT, Instituto de Ecología, A.C., Red de Estudios Moleculares Avanzados, kilómetro 2.5 Ant. Carretera a Coatepec, Xalapa, Veracruz 91070, Mexico.
B Instituto de Biología, Universidad Nacional Autónoma de México, C.P. 04510, Apartadod Postal 70-153, Ciudad Universitaria, Ciudad de México, Mexico.
C Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05 České Budějovice, Czech Republic.
D Current address: Escuela Nacional de Estudios Superiores Unidad Mérida (ENES-Mérida), Universidad Nacional Autónoma de México, kilómetro 4.5 Carretera Mérida-Tétiz, Municipio de Ucú, C.P. 97357, Yucatán, Mexico.
E Corresponding author. Email: ppdleon@enesmerida.unam.mx
Invertebrate Systematics 35(7) 754-775 https://doi.org/10.1071/IS21007
Submitted: 2 February 2021 Accepted: 3 April 2021 Published: 23 September 2021
Abstract
Phyllodistomum is one of the most species-rich genera of parasitic platyhelminths, with 120 species described worldwide; they infect the urinary bladder of marine and freshwater fishes. As the number of new species within the genus has increased, morphological conservatism, and the lack of reliable diagnostic traits make the separation of species a challenging task. The increase of genetic data for Phyllodistomum species has permitted the use of an integrative taxonomy approach as a framework for species discovery and delimitation. DNA sequences (28S rRNA and COI mtDNA) were obtained from individuals of Phyllodistomum sampled in 29 locations across Middle America, and used in combination with morphology, host association and geographic distribution to uncover five new congeneric species. Morphologically, the new species are relatively similar; there are no unique morphological traits to readily distinguish them. We first investigated species boundaries through phylogenetic analyses of the independent and concatenated datasets; analyses recognised five candidate species showing reciprocal monophyly and strong clade support, particularly for COI data. The interspecific 28S rRNA and COI sequence divergence among the new species from 0.4 to 18.4% and from 5.1 to 27% respectively. These results were further validated by a Bayesian species delimitation approach. The five new species are well supported by molecular data used in combination with other sources of information such as host association and geographical distribution and are described herein as Phyllodistomum romualdae sp. nov., P. virmantasi sp. nov., P. isabelae sp. nov., P. scotti sp. nov., and P. simonae sp. nov.
Keywords: 28S rRNA, Bayesian Phylogenetics and Phylogeography, COI, Gorgoderidae, integrative taxonomy, Phyllodistomum, Platyhelminthes, Trematoda.
References
Abdel-Gaber, R., Al Quraishy, S., Dkhil, M. A. M., Abu Hawsah, M., Alghamdi, M., Althomali, A., Bakr, L., Maher, S., and El-Mallah, A. (2020). Phyllodistomum vaili (Plagiorchiida: Gorgoderidae) infecting Parupeneus rubescens (Perciformes: Mullidae): morphology and phylogeny. Revista Brasileira de Parasitologia Veterinária 29, e020019.| Phyllodistomum vaili (Plagiorchiida: Gorgoderidae) infecting Parupeneus rubescens (Perciformes: Mullidae): morphology and phylogeny.Crossref | GoogleScholarGoogle Scholar | 32236335PubMed |
Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.
| A new look at the statistical model identification.Crossref | GoogleScholarGoogle Scholar |
American Veterinary Medical Association (2013). ‘American Veterinary Medical Association: Guidelines for the Euthanasia of Animals.’ (AVMA: Schaumburg, IL, USA.)
Blasco-Costa, I., Faltynková, A., Georgieva, S., Skírnisson, K., Scholz, T., and Kostadinova, A. (2014). Fish pathogens near the Arctic Circle: molecular, morphological and ecological evidence for unexpected diversity of Diplostomum (Digenea: Diplostomidae) in Iceland. International Journal for Parasitology 44, 703–715.
| Fish pathogens near the Arctic Circle: molecular, morphological and ecological evidence for unexpected diversity of Diplostomum (Digenea: Diplostomidae) in Iceland.Crossref | GoogleScholarGoogle Scholar | 24929135PubMed |
Bowles, J., Blair, D., and McManus, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.
| Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing.Crossref | GoogleScholarGoogle Scholar | 1435857PubMed |
Campbell, R. A. (2008). Family Gorgoderidae Looss, 1899. In ‘Keys to the Trematoda’. (Eds R. A. Bray, D. I. Gibson, and A. Jones.) Vol. 3, pp. 191–214. (CAB International: Wallingford, UK.)
Carstens, B. C., Pelletier, T. A., Reid, N. M., and Satler, J. D. (2013). How to fail at species delimitation. Molecular Ecology 22, 4369–4383.
| How to fail at species delimitation.Crossref | GoogleScholarGoogle Scholar | 23855767PubMed |
Chambers, E. A., and Hillis, D. M. (2020). The multispecies coalescent over-splits species in the case of geographically widespread taxa. Systematic Biology 69, 184–193.
| The multispecies coalescent over-splits species in the case of geographically widespread taxa.Crossref | GoogleScholarGoogle Scholar | 31180508PubMed |
Choudhury, A., Aguirre-Macedo, M. L., Curran, S. S., Ostrowski de Núñez, M., Overstreet, R. M., Pérez-Ponce de León, G., and Portes Santos, C. (2016). Trematode diversity in freshwater fishes of the Globe II: ‘New World’. Systematic Parasitology 93, 271–282.
| Trematode diversity in freshwater fishes of the Globe II: ‘New World’.Crossref | GoogleScholarGoogle Scholar | 26898590PubMed |
Choudhury, A., García-Varela, M., and Pérez-Ponce de León de León, G. (2017). Parasites of freshwater fishes and the Great American Biotic Interchange: a bridge too far? Journal of Helminthology 91, 174–196.
| Parasites of freshwater fishes and the Great American Biotic Interchange: a bridge too far?Crossref | GoogleScholarGoogle Scholar | 27376756PubMed |
Cutmore, S. C., and Cribb, T. H. (2018). Two species of Phyllodistomum Braun, 1899 (Trematoda: Gorgoderidae) from Moreton Bay, Australia. Systematic Parasitology 95, 325–336.
| Two species of Phyllodistomum Braun, 1899 (Trematoda: Gorgoderidae) from Moreton Bay, Australia.Crossref | GoogleScholarGoogle Scholar | 29417344PubMed |
Cutmore, S. C., Miller, T. L., Curran, S. S., Bennett, M. B., and Cribb, T. H. (2013). Phylogenetic relationships of the Gorgoderidae (Platyhelminthes: Trematoda), including the proposal of a new subfamily (Degeneriinae n. subfam.). Parasitology Research 112, 3063–3074.
| Phylogenetic relationships of the Gorgoderidae (Platyhelminthes: Trematoda), including the proposal of a new subfamily (Degeneriinae n. subfam.).Crossref | GoogleScholarGoogle Scholar | 23760874PubMed |
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 22847109PubMed |
Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society. Linnean Society of London 85, 407–415.
| Towards integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |
de Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology 56, 879–886.
| Species concepts and species delimitation.Crossref | GoogleScholarGoogle Scholar | 18027281PubMed |
Dejaco, T., Gassner, M., Arthrofer, W., Schlick-Steiner, B., and Steiner, F. M. (2016). Taxonomist’s nightmare … evolutionist’s delight: an integrative approach resolves species limits in jumping bristletails despite widespread hybridization and parthenogenesis. Systematic Biology 65, 947–974.
| Taxonomist’s nightmare … evolutionist’s delight: an integrative approach resolves species limits in jumping bristletails despite widespread hybridization and parthenogenesis.Crossref | GoogleScholarGoogle Scholar | 26869489PubMed |
Eberle, J., Bazzato, E., Fabrizi, S., Rossini, M., Colomba, M., Cillo, D., Uliana, M., Spáracio, I., Sabatinelli, G., Warnock, R. C. M., Carpaneto, G., and Ahrens, D. (2019). Sex-biased dispersal obscures species boundaries in integrative species delimitation approaches. Systematic Biology 68, 441–459.
| Sex-biased dispersal obscures species boundaries in integrative species delimitation approaches.Crossref | GoogleScholarGoogle Scholar | 30364986PubMed |
García-Varela, M., and Nadler, S. A. (2005). Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. The Journal of Parasitology 91, 1401–1409.
| Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences.Crossref | GoogleScholarGoogle Scholar | 16539024PubMed |
Gordy, M. A., Locke, S. A., Rawlings, T. A., Lapierre, A. R., and Hanington, P. C. (2017). Molecular and morphological evidence for nine species in North American Australapatemon (Sudarikov, 1959): a phylogeny expansion with description of the zygocercous Australapatemon mclaughlini n. sp. Parasitology Research 116, 2181–2198.
| Molecular and morphological evidence for nine species in North American Australapatemon (Sudarikov, 1959): a phylogeny expansion with description of the zygocercous Australapatemon mclaughlini n. sp.Crossref | GoogleScholarGoogle Scholar | 28623502PubMed |
Herrmann, K. K., Poulin, R., Keeney, D. B., and Blasco-Costa, I. (2014). Genetic structure in a progenetic trematode: signs of cryptic species with contrasting reproductive strategies. International Journal for Parasitology 44, 811–818.
| Genetic structure in a progenetic trematode: signs of cryptic species with contrasting reproductive strategies.Crossref | GoogleScholarGoogle Scholar | 25058509PubMed |
Ho, H. W., Bray, R. A., Cutmore, S. C., Ward, S., and Cribb, T. H. (2014). Two new species of Phyllodistomum Braun, 1899 (Trematoda: Gorgoderidae Looss, 1899) from Great Barrier Reef fishes. Zootaxa 3779, 551–562.
| Two new species of Phyllodistomum Braun, 1899 (Trematoda: Gorgoderidae Looss, 1899) from Great Barrier Reef fishes.Crossref | GoogleScholarGoogle Scholar | 24871750PubMed |
Karanovic, T., Djurakic, M., and Eberhard, S. M. (2016). Cryptic species or inadequate taxonomy? Implementation of 2D geometric morphometrics based on integumental organs as landmarks for delimitation and description of copepod taxa. Systematic Biology 65, 304–327.
| Cryptic species or inadequate taxonomy? Implementation of 2D geometric morphometrics based on integumental organs as landmarks for delimitation and description of copepod taxa.Crossref | GoogleScholarGoogle Scholar | 26608965PubMed |
Kohn, A., Fernandes, B. M. N., and Cohen, S. C. (2007). ‘South American Trematodes Parasites of Fishes.’ (Editora Imprinta: Rio de Janeiro, Brazil.)
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar | 27004904PubMed |
Leaché, A. D., and Fujita, M. K. (2010). Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings of the Royal Society of London – B. Biological Sciences 277, 3071–3077.
| Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus).Crossref | GoogleScholarGoogle Scholar |
López, Z., Cardenas, L., Runil, F., and González, M. T. (2015). Contrasting definitive hosts as determinants of the genetic structure in a parasite with complex life cycle along the south‐eastern Pacific. Molecular Ecology 24, 1060–1073.
| Contrasting definitive hosts as determinants of the genetic structure in a parasite with complex life cycle along the south‐eastern Pacific.Crossref | GoogleScholarGoogle Scholar | 25602037PubMed |
Martínez-Aquino, A., Ceccarelli, F. S., and Pérez-Ponce de León, G. (2013). Molecular phylogeny of the genus Margotrema (Digenea: Allocreadiidae), parasitic flatworms of goodeid freshwater fishes across central Mexico: species boundaries, host-specificity, and geographical congruence. Zoological Journal of the Linnean Society 168, 1–16.
| Molecular phylogeny of the genus Margotrema (Digenea: Allocreadiidae), parasitic flatworms of goodeid freshwater fishes across central Mexico: species boundaries, host-specificity, and geographical congruence.Crossref | GoogleScholarGoogle Scholar |
Mendoza-Garfias, B., and Pérez-Ponce de León, G. (2005). Phyllodistomum centropomi sp. n. (Digenea: Gorgoderidae), a parasite of the fat snook, Centropomus parallelus (Osteichthyes: Centropomidae), in the Papaloapan River at Tlacotalpan, Veracruz State, Mexico. Zootaxa 1056, 43–51.
| Phyllodistomum centropomi sp. n. (Digenea: Gorgoderidae), a parasite of the fat snook, Centropomus parallelus (Osteichthyes: Centropomidae), in the Papaloapan River at Tlacotalpan, Veracruz State, Mexico.Crossref | GoogleScholarGoogle Scholar |
Morcillo, F., Ornelas-García, C. P., Alcaraz, L., Matamoros, W., and Doadrio, I. (2016). Phylogenetic relationships and evolutionary history of the Mesoamerican endemic freshwater fish family Profundulidae (Cyprinodontiformes: Actinopterygii). Molecular Phylogenetics and Evolution 94, 242–251.
| Phylogenetic relationships and evolutionary history of the Mesoamerican endemic freshwater fish family Profundulidae (Cyprinodontiformes: Actinopterygii).Crossref | GoogleScholarGoogle Scholar | 26364972PubMed |
Nadler, S. A., and Hudspeth, D. S. (1998). Ribosomal DNA and phylogeny of the Ascaridoidea (Nemata: Secernentea): implications for morphological evolution and classification. Molecular Phylogenetics and Evolution 10, 221–236.
| Ribosomal DNA and phylogeny of the Ascaridoidea (Nemata: Secernentea): implications for morphological evolution and classification.Crossref | GoogleScholarGoogle Scholar | 9878233PubMed |
Nakao, M. (2015). Phyllodistomum kanae sp. nov. (Trematoda: Gorgoderidae), a bladder fluke from the Ezo salamander Hynobius retardatus. Parasitology International 64, 314–318.
| Phyllodistomum kanae sp. nov. (Trematoda: Gorgoderidae), a bladder fluke from the Ezo salamander Hynobius retardatus.Crossref | GoogleScholarGoogle Scholar | 25892565PubMed |
Oliva, M. E., Valdivia, I. M., Chavez, R. A., Molina, H., and Cárdenas, L. (2015). Molecular and morphological evidence demonstrating two species of Helicometrina Linton 1910 (Digenea: Opecoelidae) in northern Chile. The Journal of Parasitology 101, 694–700.
| Molecular and morphological evidence demonstrating two species of Helicometrina Linton 1910 (Digenea: Opecoelidae) in northern Chile.Crossref | GoogleScholarGoogle Scholar | 26221995PubMed |
Ostrowski de Núñez, M., Arredondo, N. J., and Gil de Pertierra, A. (2017). Adult trematodes (Platyhelminthes) of freshwater fishes from Argentina: a checklist. Revue Suisse de Zoologie 124, 91–113.
Pante, E., Schoelinck, C., and Puillandre, N. (2015). From integrative taxonomy to species description: one step beyond. Systematic Biology 64, 152–160.
| From integrative taxonomy to species description: one step beyond.Crossref | GoogleScholarGoogle Scholar | 25358968PubMed |
Pérez-Ponce de León, G., and Hernández-Mena, D. I. (2019). Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ Tree of Life. Journal of Helminthology 93, 260–276.
| Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ Tree of Life.Crossref | GoogleScholarGoogle Scholar | 30973318PubMed |
Pérez Ponce de León, G., García Prieto, L., and Mendoza-Garfías, B. (2007). Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534, 1–247.
| Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico.Crossref | GoogleScholarGoogle Scholar |
Pérez-Ponce de León, G., Martinez-Aquino, A., and Mendoza-Garfias, B. (2015a). Two new species of Phyllodistomum Braun, 1899 (Digenea: Gorgoderidae), from freshwater fishes (Cyprinodontiformes: Goodeidae: Goodeinae) in central Mexico: an integrative taxonomy approach using morphology, ultrastructure and molecular phylogenetics. Zootaxa 4013, 87–99.
| Two new species of Phyllodistomum Braun, 1899 (Digenea: Gorgoderidae), from freshwater fishes (Cyprinodontiformes: Goodeidae: Goodeinae) in central Mexico: an integrative taxonomy approach using morphology, ultrastructure and molecular phylogenetics.Crossref | GoogleScholarGoogle Scholar | 26623884PubMed |
Pérez-Ponce de León, G., Pinacho-Pinacho, C. D., Mendoza-Garfias, B., and García-Varela, M. (2015b). 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 Parasitologica 60, 298–307.
| 26203999PubMed |
Pérez-Ponce de León, G., Garcia-Varela, M., Pinacho-Pinacho, C. D., Sereno-Uribe, A. L., and Poulin, R. (2016). Species delimitation in trematodes using DNA sequences: Middle-American Clinostomum as a case study. Parasitology 143, 1773–1789.
| Species delimitation in trematodes using DNA sequences: Middle-American Clinostomum as a case study.Crossref | GoogleScholarGoogle Scholar | 27571850PubMed |
Petkevičiūtė, R., Stunžėnas, V., Stanevičiūtė, G., and Zhokhov, A. E. (2015). European Phyllodistomum (Digenea, Gorgoderidae) and phylogenetic affinities of Cercaria duplicata based on rDNA and karyotypes. Zoologica Scripta 44, 191–202.
| European Phyllodistomum (Digenea, Gorgoderidae) and phylogenetic affinities of Cercaria duplicata based on rDNA and karyotypes.Crossref | GoogleScholarGoogle Scholar |
Petkevičiūtė, R., Zhokhov, A. E., Stunžėnas, V., Poddubnaya, L. G., and Stanevičiūtė, G. (2020). Phyllodistomum kupermani n. sp. from the European perch, Perca fluviatilis L. (Perciformes: Percidae), and redescription of Phyllodistomum macrocotyle (Lühe, 1909) with notes on the species diversity and host specificity in the European Phyllodistomum spp. (Trematoda: Gorgoderidae). Parasites & Vectors 13, 561.
| Phyllodistomum kupermani n. sp. from the European perch, Perca fluviatilis L. (Perciformes: Percidae), and redescription of Phyllodistomum macrocotyle (Lühe, 1909) with notes on the species diversity and host specificity in the European Phyllodistomum spp. (Trematoda: Gorgoderidae).Crossref | GoogleScholarGoogle Scholar |
Puillandre, N., Lambert, A., Brouillet, S., and Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.
| ABGD, Automatic Barcode Gap Discovery for primary species delimitation.Crossref | GoogleScholarGoogle Scholar | 21883587PubMed |
Rannala, B., and Yang, Z. (2013). Improved reversible jump algorithms for Bayesian species delimitation. Genetics 194, 245–253.
| Improved reversible jump algorithms for Bayesian species delimitation.Crossref | GoogleScholarGoogle Scholar | 23502678PubMed |
Rannala, B., and Yang, Z. (2017). Efficient Bayesian species tree inference under the multispecies coalescent. Systematic Biology 66, 823–842.
| Efficient Bayesian species tree inference under the multispecies coalescent.Crossref | GoogleScholarGoogle Scholar | 28053140PubMed |
Rannala, B., and Yang, Z. (2020). Species delimitation. In ‘Phylogenetics in the Genomic Era’. (Eds C. Scornavacca, F. Delsuc, and N. Galtier.) pp. 5.5:1–5.5:18. Available at https://hal.archives-ouvertes.fr/hal-02536468
Razo-Mendivil, U., Pérez-Ponce de León, G., and Rubio-Godoy, M. (2013). Integrative taxonomy identifies a new species of Phyllodistomum (Digenea: Gorgoderidae) from the two spot livebearer, Heterandria bimaculata (Teleostei: Poeciliidae), in central Veracruz, Mexico. Parasitology Research 112, 4137–4150.
| Integrative taxonomy identifies a new species of Phyllodistomum (Digenea: Gorgoderidae) from the two spot livebearer, Heterandria bimaculata (Teleostei: Poeciliidae), in central Veracruz, Mexico.Crossref | GoogleScholarGoogle Scholar | 24022129PubMed |
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |
Rosas-Valdez, R., and 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. Revista Mexicana de Biodiversidad 79, 473–499.
Rosas-Valdez, R., Choudhury, A., and Pérez-Ponce de León, G. (2011). Molecular prospecting for cryptic species in Phyllodistomum lacustri (Platyhelminthes, Gorgoderidae). Zoologica Scripta 40, 296–305.
| Molecular prospecting for cryptic species in Phyllodistomum lacustri (Platyhelminthes, Gorgoderidae).Crossref | GoogleScholarGoogle Scholar |
Sites, J. W., and Marshall, J. C. (2003). Delimiting species: a Renaissance issue in systematic biology. Trends in Ecology & Evolution 18, 462–470.
| Delimiting species: a Renaissance issue in systematic biology.Crossref | GoogleScholarGoogle Scholar |
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 16928733PubMed |
Stunžėnas, V., Petkevičiūtė, R., Poddubnaya, L. G., Stanevičiūtė, G., and Zhokhov, A. E. (2017). Host specificity, molecular phylogeny and morphological differences of Phyllodistomum pseudofolium Nybelin, 1926 and Phyllodistomum angulatum Linstow, 1907 (Trematoda: Gorgoderidae) with notes on Eurasian ruffe as final host for Phyllodistomum spp. Parasites & Vectors 10, 286.
| Host specificity, molecular phylogeny and morphological differences of Phyllodistomum pseudofolium Nybelin, 1926 and Phyllodistomum angulatum Linstow, 1907 (Trematoda: Gorgoderidae) with notes on Eurasian ruffe as final host for Phyllodistomum spp.Crossref | GoogleScholarGoogle Scholar |
Sukumaran, J., and Knowles, L. L. (2017). Multispecies coalescent delimits structure, not species. Proceedings of the National Academy of Sciences of the United States of America 114, 1607–1612.
| Multispecies coalescent delimits structure, not species.Crossref | GoogleScholarGoogle Scholar | 28137871PubMed |
Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.
| CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Crossref | GoogleScholarGoogle Scholar | 7984417PubMed |
Urabe, M., Ishibashi, R., and Uehara, K. (2015). The life cycle and molecular phylogeny of a gorgoderid trematode recorded from the mussel Nodularia douglasiae in the Yodo River, Japan. Parasitology International 64, 26–32.
| The life cycle and molecular phylogeny of a gorgoderid trematode recorded from the mussel Nodularia douglasiae in the Yodo River, Japan.Crossref | GoogleScholarGoogle Scholar | 25220581PubMed |
Vidal-Martínez, V. M., Aguirre-Macedo, M. L., Scholz, T., González-Solís, D., and Mendoza-Franco, E. F. (2001). ‘Atlas of the Helminth Parasites of Cichlid Fish of México.’ (Academia: Praha, Czech Republic.)
Yang, Z. (2002). Likelihood and Bayes estimation of ancestral population sizes in hominoids using data from multiple loci. Genetics 162, 1811–1823.
| Likelihood and Bayes estimation of ancestral population sizes in hominoids using data from multiple loci.Crossref | GoogleScholarGoogle Scholar | 12524351PubMed |
Yang, Z. (2015). The BPP program for species tree estimation and species delimitation. Current Zoology 61, 854–865.
| The BPP program for species tree estimation and species delimitation.Crossref | GoogleScholarGoogle Scholar |
Yang, Z., and Rannala, B. (2010). Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences of the United States of America 107, 9264–9269.
| Bayesian species delimitation using multilocus sequence data.Crossref | GoogleScholarGoogle Scholar | 20439743PubMed |
Yang, Z., and Rannala, B. (2014). Unguided species delimitation using DNA sequence data from multiple loci. Molecular Biology and Evolution 31, 3125–3135.
| Unguided species delimitation using DNA sequence data from multiple loci.Crossref | GoogleScholarGoogle Scholar | 25274273PubMed |
Zhang, C., Zhang, D. X., Zhu, T., and Yang, Z. (2011). Evaluation of a Bayesian coalescent method of species delimitation. Systematic Biology 60, 747–761.
| Evaluation of a Bayesian coalescent method of species delimitation.Crossref | GoogleScholarGoogle Scholar | 21876212PubMed |
Zhang, J., Kapli, P., Pavlidis, P., and Stamatakis, A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.
| A general species delimitation method with applications to phylogenetic placements.Crossref | GoogleScholarGoogle Scholar | 23990417PubMed |
