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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Integrative taxonomy increases biodiversity knowledge of Gusana (Platyhelminthes, Tricladida, Geoplanidae) with the description of four new Chilean species

Ana Laura Almeida A , Marta Álvarez-Presas B , Laura Bolonhezi C and Fernando Carbayo https://orcid.org/0000-0002-8524-9715 A C *
+ Author Affiliations
- Author Affiliations

A Museu de Zoologia da Universidade de São Paulo, Avenida Nazaré, 481, CEP 04263-000, Ipiranga, São Paulo, SP, Brazil.

B School of Biological Sciences, University of Bristol, 24 Tyndall Avenue, BS8 1TQ, Bristol, UK.

C Laboratório de Ecologia e Evolução, Escola de Artes, Ciências e Humanidades, Universidade de São Paulo - USP, Avenida Arlindo Bettio, 1000, CEP 03828-000, São Paulo, SP, Brazil.

* Correspondence to: baz@usp.br

Handling Editor: Katrine Worsaae

Invertebrate Systematics 36(6) 533-556 https://doi.org/10.1071/IS21066
Submitted: 18 September 2021  Accepted: 3 February 2022   Published: 18 July 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

The Chilean land planarian genus Gusana (Platyhelminthes, Tricladida, Geoplaninae) currently comprises three species that were described in the 19th century. Four new species of the genus are described herein, namely G. hualpensis Carbayo, sp. nov., G. lujanae Almeida & Carbayo, sp. nov., G. melipeucensis Almeida & Carbayo, sp. nov. and G. purensis Bolonhezi, Almeida & Carbayo, sp. nov. An integrative taxonomy approach was adopted by combining morphological (anatomy, histology) and molecular (COI and 28S genes) information. Additionally, the monophyletic status of Gusana is investigated and the species are delimited by a recently introduced molecular delimitation method based on pairwise genetic distances. All Gusana species are very similar in attributes such as body shape, dorsal colour pattern and internal organs, namely the pharynx and copulatory apparatus and only differ in the details. Gusana is retrieved as monophyletic and the molecular delimitation method recovered the same species recognised morphologically. A re-diagnosis of the genus and replacement of G. lata into Pseudogeoplana are also proposed. A new role of the penis papilla is also suggested based on the spermatophore found in Gusana lujanae.

Keywords: ASAP, Chile, flatworms, Geoplanidae, morphology, Neotropical, phylogeny, systematics.


References

Almeida, AL, Francoy, TM, Álvarez-Presas, M, and Carbayo, F (2021). Convergent evolution: A new subfamily for bipaliin-like Chilean land planarians (Platyhelminthes). Zoologica Scripta 50, 500–508.
Convergent evolution: A new subfamily for bipaliin-like Chilean land planarians (Platyhelminthes).Crossref | GoogleScholarGoogle Scholar |

Álvarez-Presas, M, Carbayo, F, Rozas, J, and Riutort, M (2011). Land planarians (Platyhelminthes) as a model organism for finescale phylogeographic studies: understanding patterns of biodiversity in the Brazilian Atlantic Forest hotspot. Journal of Evolutionary Biology 24, 887–896.
Land planarians (Platyhelminthes) as a model organism for finescale phylogeographic studies: understanding patterns of biodiversity in the Brazilian Atlantic Forest hotspot.Crossref | GoogleScholarGoogle Scholar | 21288273PubMed |

Álvarez-Presas, M, Mateos, E, Tudó, À, Jones, H, and Riutort, M (2014). Diversity of introduced terrestrial flatworms in the Iberian Peninsula: a cautionary tale. PeerJ 2, e430.
Diversity of introduced terrestrial flatworms in the Iberian Peninsula: a cautionary tale.Crossref | GoogleScholarGoogle Scholar | 24949245PubMed |

Araujo, APG, Carbayo, F, Riutort, M, and Álvarez-Presas, M (2020). Five new pseudocryptic land planarian species of Cratera (Platyhelminthes: Tricladida) unveiled through integrative taxonomy. PeerJ 8, e9726.
Five new pseudocryptic land planarian species of Cratera (Platyhelminthes: Tricladida) unveiled through integrative taxonomy.Crossref | GoogleScholarGoogle Scholar | 32983634PubMed |

Boll, PK, Do Amaral, SV, and Leal-Zanchet, AM (2019). Two new land planarian species (Platyhelminthes: Tricladida: Geoplanidae) from protected areas in southern Brazil. Zootaxa 4664, 535–550.
Two new land planarian species (Platyhelminthes: Tricladida: Geoplanidae) from protected areas in southern Brazil.Crossref | GoogleScholarGoogle Scholar |

Capella-Gutiérrez, S, Silla-Martínez, JM, and Gabaldón, T (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973.
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 19505945PubMed |

Carbayo, F, Álvarez-Presas, M, Olivares, CT, Marques, FPL, Froehlich, EM, and Riutort, M (2013). Molecular phylogeny of Geoplaninae (Platyhelminthes) challenges current classification: proposal of taxonomic actions. Zoologica Scripta 42, 508–528.
Molecular phylogeny of Geoplaninae (Platyhelminthes) challenges current classification: proposal of taxonomic actions.Crossref | GoogleScholarGoogle Scholar |

Cason, JE (1950). A rapid one-step Mallory–Heidenhain stain for connective tissue. Stain Technology 25, 225–226.
A rapid one-step Mallory–Heidenhain stain for connective tissue.Crossref | GoogleScholarGoogle Scholar | 14782060PubMed |

Chisholm, LA, Morgan, JAT, Adlard, RD, and Whittington, ID (2001). Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. International Journal for Parasitology 31, 1253–1263.
Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences.Crossref | GoogleScholarGoogle Scholar | 11513895PubMed |

de Souza, SA, and Leal-Zanchet, AM (2004). Histological and histochemical characterization of the secretory cells of Choeradoplana iheringi Graff, 1899 (Platyhelminthes: Tricladida: Terricola). Brazilian Journal of Biology 64, 511–522.
Histological and histochemical characterization of the secretory cells of Choeradoplana iheringi Graff, 1899 (Platyhelminthes: Tricladida: Terricola).Crossref | GoogleScholarGoogle Scholar |

Ewing, B, and Green, P (1998). Base-calling of automated sequencer traces using Phred II. Error probabilities. Genome Research 8, 186–194.
Base-calling of automated sequencer traces using Phred II. Error probabilities.Crossref | GoogleScholarGoogle Scholar | 9521922PubMed |

Ewing, B, Hillier, L, Wendl, MC, and Green, P (1998). Base-calling of automated sequencer traces using Phred I. Accuracy assessment. Genome Research 8, 175–185.
Base-calling of automated sequencer traces using Phred I. Accuracy assessment.Crossref | GoogleScholarGoogle Scholar | 9521921PubMed |

Fetzner, JW (1999). Extracting high-quality DNA from shed reptiles skins: a simplified method. BioTechniques 26, 1052–1054.
Extracting high-quality DNA from shed reptiles skins: a simplified method.Crossref | GoogleScholarGoogle Scholar | 10376138PubMed |

Froehlich, CG (1956). Tricladida Terricola das regiões de Teresópolis e Ubatuba. Papéis Avulsos do Departamento de Zoologia 12, 313–344.

Froehlich, CG (1959). On geoplanids from Brazil. Boletim da Faculdade de Filosofia. Ciências e Letras da Universidade de São Paulo 22, 201–242.

Froehlich, CG (1967). A contribution on the zoogeography of neotropical land planarians. Acta Zoológica Lilloana 23, 153–162.

Froehlich, EM (1978). On a collection of Chilean land planarians. Boletins de Zoologia da Universidade de São Paulo 3, 7–80.

Froehlich, EM, and Froehlich, CG (1972). Land planarians from the Amazonian region. Papéis Avulsos de Zoologia 26, 29–45.

Gordon, D, Abajian, C, and Green, P (1998). Consed: a graphical tool for sequence finishing. Genome Research 8, 195–202.
Consed: a graphical tool for sequence finishing.Crossref | GoogleScholarGoogle Scholar | 9521923PubMed |

Gordon, D, Desmarais, C, and Green, P (2001). Automated finishing with autofinish. Genome Research 11, 614–625.
Automated finishing with autofinish.Crossref | GoogleScholarGoogle Scholar | 11282977PubMed |

Hall, TA (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT.Crossref | GoogleScholarGoogle Scholar |

Heinzel, L (1929). Zur Kenntnis der Rhynchodemiden. Zoologische Jahrbucher. Abteilung fur Systematik, Ökologie und Geographie der Tiere 56, 425–462.

Heneberg, P, and Literák, I (2013). Molecular phylogenetic characterization of Collyriclum faba with reference to its three host-specific ecotypes. Parasitology International 62, 262–267.
Molecular phylogenetic characterization of Collyriclum faba with reference to its three host-specific ecotypes.Crossref | GoogleScholarGoogle Scholar | 23337459PubMed |

Katoh K, Standley DM (2014) MAFFT: iterative refinement and additional methods. In ‘Multiple Sequence Alignment Methods, Methods in Molecular Biology’. (Ed. DJ Russell) pp. 131–146. (Springer Science+Business Media, LLC)
| Crossref |

Lago-Barcia, D, Silva, MS, and Carbayo, F (2021). Revision and description of six species of Choeradoplana (Platyhelminthes, Tricladida), with an emendation to the genus. ZooKeys 1016, 1–48.
Revision and description of six species of Choeradoplana (Platyhelminthes, Tricladida), with an emendation to the genus.Crossref | GoogleScholarGoogle Scholar | 33628077PubMed |

Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T, and Calcott, B (2017). Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
Partitionfinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 28013191PubMed |

Lázaro, EM, Sluys, R, Pala, M, Stocchino, GA, Baguñà, J, and Riutort, M (2009). Molecular barcoding and phylogeography of sexual and asexual freshwater planarians of the genus Dugesia in the Western Mediterranean (Platyhelminthes, Tricladida, Dugesiidae). Molecular Phylogenetics and Evolution 52, 835–845.
Molecular barcoding and phylogeography of sexual and asexual freshwater planarians of the genus Dugesia in the Western Mediterranean (Platyhelminthes, Tricladida, Dugesiidae).Crossref | GoogleScholarGoogle Scholar | 19435604PubMed |

Leal-Zanchet, AM, and Froehlich, EM (2006). A species complex in the genus Notogynaphallia Ogren & Kawakatsu (Platyhelminthes: Tricladida: Terricola) with a taxonomic revision of homonyms of Geoplana marginata Schultze & Müller and a reinterpretation of Notogynaphallia caissara (Froehlich) anatomy. Belgian Journal of Zoology 136, 81–100.

Littlewood, DTJ, Rohde, K, and Clough, KA (1997). Parasite speciation within or between host species? Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27, 1289–1297.
Parasite speciation within or between host species? Phylogenetic evidence from site-specific polystome monogeneans.Crossref | GoogleScholarGoogle Scholar |

Marcus, E (1954). Reports of the Lund University Chile Expedition 1948–1949. 11. Turbellaria, Lunds Universitets Årsskrift 49, 3–114.

Minh, BQ, Schmidt, HA, Chernomor, O, Schrempf, D, Woodhams, MD, von Haeseler, A, and Lanfear, R (2020). IQ-TREE 2: new models and efficient methods for phylogenetic inference in the Genomic Era. Molecular Biology and Evolution 37, 1530–1534.
IQ-TREE 2: new models and efficient methods for phylogenetic inference in the Genomic Era.Crossref | GoogleScholarGoogle Scholar | 32011700PubMed |

Negrete, L, Gira, RD, and Brusa, F (2019). Two new species of land planarians (Platyhelminthes, Tricladida, Geoplanidae) from protected areas in the southern extreme of the Paranaense Rainforest, Argentina. Zoologischer Anzeiger 279, 38–51.
Two new species of land planarians (Platyhelminthes, Tricladida, Geoplanidae) from protected areas in the southern extreme of the Paranaense Rainforest, Argentina.Crossref | GoogleScholarGoogle Scholar |

Negrete, L, Álvarez-Presas, M, Riutort, M, and Brusa, F (2021). Integrative taxonomy of land planarians (Platyhelminthes: Geoplanidae) from the Andean–Patagonian forests from Argentina and Chile, with the erection of two new genera. Journal of Zoological Systematics and Evolutionary Research 59, 588–612.
Integrative taxonomy of land planarians (Platyhelminthes: Geoplanidae) from the Andean–Patagonian forests from Argentina and Chile, with the erection of two new genera.Crossref | GoogleScholarGoogle Scholar |

Ogren, RE, and Kawakatsu, M (1990). Index to the species of the family Geoplanidae (Turbellaria, Tricladida, Terricola) Part I: Geoplaninae. The Bulletin of Fuji Women’s College 28, 79–166.

Puillandre, N, Brouillet, S, and Achaz, G (2021). ASAP: assemble species by automatic partitioning. Molecular Ecology Resources 21, 609–620.
ASAP: assemble species by automatic partitioning.Crossref | GoogleScholarGoogle Scholar | 33058550PubMed |

Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larger, B, Liu, L, Suchard, MA, and Huelsenbeck, JP (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 |

Sandison, AT (1955). The histological examination of mummified material. Stain Technology 30, 277–283.
The histological examination of mummified material.Crossref | GoogleScholarGoogle Scholar | 13274233PubMed |

Sluys, R, Neumann, M, de Lima, RF, and Drewes, RC (2017). Land flatworms (Platyhelminthes, Geoplanidae) of São Tomé: a first account on their diversity, with the description of five new species. Zootaxa 4221, 291–322.
Land flatworms (Platyhelminthes, Geoplanidae) of São Tomé: a first account on their diversity, with the description of five new species.Crossref | GoogleScholarGoogle Scholar |

Sunnucks, P, Blacket, MJ, Taylor, JM, Sands, CJ, Ciavaglia, SA, Garrick, RC, Tait, NN, Rowell, DM, and Pavlova, A (2006). A tale of two flatties: different responses of two terrestrial flatworms to past environmental climatic fluctuations at Tallaganda in montane southeastern Australia. Molecular Ecology 15, 4513–4531.
A tale of two flatties: different responses of two terrestrial flatworms to past environmental climatic fluctuations at Tallaganda in montane southeastern Australia.Crossref | GoogleScholarGoogle Scholar | 17107480PubMed |

Tkach, V, Grabda-Kazubska, B, Pawlowski, J, and Swiderski, Z (1999). Molecular and morphological evidence for close phylogenetic affinities of the genera Macrodera, Lepdophallus, Metaleptophallus and Paralepoderma (Digenea, Plagiorchiata). Acta Parasitologica 44, 170–179.

Vila-Farré, M, Sluys, R, Mateos, E, Jones, HD, and Romero, R (2011). Land planarians (Platyhelminthes: Tricladida: Geoplanidae) from the Iberian Peninsula: new records and description of two new species, with a discussion on ecology. Journal of Natural History 45, 869–891.
Land planarians (Platyhelminthes: Tricladida: Geoplanidae) from the Iberian Peninsula: new records and description of two new species, with a discussion on ecology.Crossref | GoogleScholarGoogle Scholar |

Von Graff L (1899) ‘Monographie der Turbellarien II. Tricladida Terricola (Landplanarien). Atlas von Achtundfünfzig Tafeln zur Monographie der Turbellarien II. Tricladida Terricola (Landplanarien). Pls. I–LVIII.’ (Wilhelm Engelmann: Leipzig, German Empire)

Williams, ST, and Ozawa, T (2006). Molecular phylogeny suggests polyphyly of both the turban shells (family Turbinidae) and the superfamily Trochoidea (Mollusca: Vetigastropoda). Molecular Phylogenetics and Evolution 39, 33–51.
Molecular phylogeny suggests polyphyly of both the turban shells (family Turbinidae) and the superfamily Trochoidea (Mollusca: Vetigastropoda).Crossref | GoogleScholarGoogle Scholar | 16483804PubMed |

Winsor, L (1998). Aspects of taxonomy and functional histology in terrestrial flatworms (Tricladida: Terricola). Pedobiologia 42, 412–432.