An integrative taxonomic approach reveals the first marine triclad (Platyhelminthes) trapped in a cave from a semiarid Neotropical environment
Stella Souza A , Marta Riutort B , Rodrigo Lopes Ferreira C and Ana Leal-Zanchet A D
+ Author Affiliations
- Author Affiliations
A Instituto de Pesquisas de Planárias and Programa de Pós-Graduacão em Biologia, Universidade do Vale do Rio dos Sinos (UNISINOS), 93022-750 São Leopoldo, Rio Grande do Sul, Brazil.
B Departament de Genètica, Microbiologia i Estadística and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Avinguda Diagonal 643, E-08028 Barcelona, Spain.
C Centro de Estudos em Biologia Subterrânea, Setor de Zoologia Geral, Departamento de Biologia, Universidade Federal de Lavras, Campus Universitário, Caixa Postal 3037, Lavras, Minas Gerais, Brazil.
D Corresponding author. Email: zanchet@unisinos.br
Invertebrate Systematics 32(3) 627-638 https://doi.org/10.1071/IS17062
Submitted: 13 July 2017 Accepted: 30 September 2017 Published: 8 May 2018
Abstract
A new genus and species of the suborder Maricola, representing the first marine triclad living in freshwater within a cave, is described. These flatworms show specialised features, such as a lack of pigmentation and eyes, indicating their troglobitic condition. Until now, cave-dwelling triclads have only been found as representatives of the other two triclad lineages. The phylogenetic trees based on 18S rRNA and 28S rRNA genes showed their sequences to form a clade situated in a rather derived position within the Maricola. Combining maximum likelihood and Bayesian analyses along with morphological studies, we undertake the first integrative description of a marine triclad. The new genus is characterised by a secondary copulatory bursa and ovaries located behind the root of the pharynx. Nevertheless, its assignment to a family of Maricola was a difficult task especially due to the paucity of unique defining morphological features of their families. The new species is found in a semiarid environment that suffered marine transgressions and regressions during the Cretaceous, which may explain the presence of this originally marine species in a freshwater cave. The restricted distribution of the new species and recent environmental conditions detected at its type locality raise major concern for its conservation.
Additional keywords: molecular taxonomy, stygofauna, Tricladida.
References
Álvarez-Presas, M., Baguñà, J., and Riutort, M. (2008). Molecular phylogeny of land and freshwater planarians (Tricladida, Platyhelminthes): from freshwater to land and back. Molecular Phylogenetics and Evolution 47, 555–568.| Molecular phylogeny of land and freshwater planarians (Tricladida, Platyhelminthes): from freshwater to land and back.Crossref | GoogleScholarGoogle Scholar |
Araripe, P. T., and Feijó, F. J. (1994). Bacia Potiguar. Boletim de Geociências da Petrobrás 8, 127–141.
Ball, I. R., and Reynoldson, T. B. (1981). ‘British Planarians.’ (Cambridge University Press: Cambridge, UK.)
Benazzi, M. (1972). Notizie preliminari sulle planarie raccolte nella seconda spedizione Lincea in Messico. Accademia Nazionale dei Lincei. Fondazione Leone Caetani 52, 403–405.
Benazzi, M. (1973). A remarkable cave planarian: Opisthobursa mexicana Benazzi, 1972. In Subterranean fauna of Mexico. Part II. Further results of the Italian zoological missions to Mexico. Problemi attuali di Scienze e di Cultura. Accademia Nazionale dei Lincei. Fondazione Leone Caetani 171, 47–54.
Benazzi, M. (1975). Opisthobursa josephinae, a new troglobitic planarian from Chiapas, Mexico. Rendiconti, Accademia Nazionale dei Lincei 8, 533–538.
Brito, I. M. (1976). História geológica das bacias sedimentares do nordeste do Brasil. Anais da Academia Brasileira de Ciencias 48, 463–474.
Carranza, S., Giribet, G., Ribera, C., Baguñà, J., and Riutort, M. (1996). Evidence that two types of rDNA coexist in the genome of Dugesia (Schmidtea) mediterranea (Playhelminthes, Turbellaria, Tricladida). Molecular Biology and Evolution 13, 824–832.
| Evidence that two types of rDNA coexist in the genome of Dugesia (Schmidtea) mediterranea (Playhelminthes, Turbellaria, Tricladida).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XktFyitbg%3D&md5=75ba07a36cfe707340f8b7b3e8e5ab22CAS |
Cassab, R. C. T. (2003). Paleontologia da Formação Jandaíra, Cretáceo Superior da Bacia Potiguar, com ênfase na Paleobiologia dos Gastrópodos. PhD Thesis, Programa de Pós-Graduação em Geologia da Universidade Federal do Rio de Janeiro, Brazil.
Charbagi-Barbirou, K., Álvarez-Presas, M., Vila, M., Gammoudi, M., Tekaya, S., and Riutort, M. (2011). Marine triclads (Platyhelminthes, Tricladida, Maricola), a preliminary molecular approach to their phylogeny. Cahiers de Biologie Marine 52, 303–311.
Claussen, D. L., Grisak, A. G., and Brown, P. F. (2003). The thermal relations of the freshwater triclad flatworm Dugesia dorotocephala (Turbellaria, Tricladida). Journal of Thermal Biology 28, 457–464.
| The thermal relations of the freshwater triclad flatworm Dugesia dorotocephala (Turbellaria, Tricladida).Crossref | GoogleScholarGoogle Scholar |
Ferreira, R. L., Xavier, P., Bernardi, L. F. O., and Souza-Silva, M. (2010). Fauna subterrânea do Estado do Rio Grande do Norte: caracterização e impactos. Revista Brasileira de Espeleologia 1, 25–51. Available at: http://www.icmbio.gov.br/revistaeletronica/index.php/RBEsp/article/view/70/59
Fišer, C., Zagmajster, M., and Ferreira, R. L. (2013). Two new amphipod families recorded in South America shed light on an old biogeographical enigma. Systematics and Biodiversity 11, 117–139.
| Two new amphipod families recorded in South America shed light on an old biogeographical enigma.Crossref | GoogleScholarGoogle Scholar |
Gourbault, N. (1978). Une nouvelle planaire primitive d’origine marine, Turbellarié Triclade de Polynésie. Cahiers de Biologie Marine 19, 23–36.
Harrath, A. H., Mansour, L., Lagnika, M., Sluys, R., Boutin, C., Alwasel, S., Poch, A., and Riutort, M. (2016). A molecular analysis of the phylogenetic position of the suborder Cavernicola within the Tricladida (Platyhelminthes), with the description of a new species of stygobiont flatworm from Benin. Zoological Journal of the Linnean Society 178, 482–491.
| A molecular analysis of the phylogenetic position of the suborder Cavernicola within the Tricladida (Platyhelminthes), with the description of a new species of stygobiont flatworm from Benin.Crossref | GoogleScholarGoogle Scholar |
Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
| MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFWisLc%3D&md5=923eb8b83abb772e70745a603d99fa8fCAS |
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 28, 1647–1649.
| Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar |
Laumer, C. E., Hejnol, A., and Giribet, G. (2015). Nuclear genomic signals of the ‘microturbellarian’ roots of platyhelminth evolutionary innovation. eLife 4, e05503.
| Nuclear genomic signals of the ‘microturbellarian’ roots of platyhelminth evolutionary innovation.Crossref | GoogleScholarGoogle Scholar |
Leal-Zanchet, A. M., Souza, S. T., and Ferreira, R. L. (2014). A new genus and species for the first recorded cave-dwelling Cavernicola (Platyhelminthes) from South America. ZooKeys 442, 1–15.
| A new genus and species for the first recorded cave-dwelling Cavernicola (Platyhelminthes) from South America.Crossref | GoogleScholarGoogle Scholar |
Mitchell, R. W., and Kawakatsu, M. (1972). A new family, genus and species of cave-adapted planarian from Mexico (Turbellaria, Tricladida, Maricola). Occasional Papers The Museum Texas Tech University 8, 1–16.
Mitchell, R. W., and Kawakatsu, M. (1973a). A new cave-adapted planarian (Tricladida, Paludicola, Planariidae) from Chiapas, Mexico. Association for Mexican Cave Studies 5, 165–170.
Mitchell, R. W., and Kawakatsu, M. (1973b). Freshwater cavernicole planarians from Mexico: new troglobitic and troglophilic Dugesia from caves of the Sierra de Guatemala (1). Annales de Spéléologie 27, 639–681.
Nimer, E. (1989). ‘Climatologia do Brasil.’ (Instituto Brasileiro de Geografia e Estatística: Rio de Janeiro, Brazil.)
Noren, M., and Jondelius, U. (2002). The phylogenetic position of the Prolecithophora (Rhabditophora, Platyhelminthes). Zoologica Scripta 31, 403–414.
| The phylogenetic position of the Prolecithophora (Rhabditophora, Platyhelminthes).Crossref | GoogleScholarGoogle Scholar |
Peel, M. C., Finlayson, B. L., and McMahon, T. A. (2007). Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences 11, 1633–1644.
Piovesan, E., Cabral, M. C., and Fauth, G. (2014). Ostracodes from the Upper Cretaceous deposits of the Potiguar Basin, northeastern Brazil: taxonomy, paleoecology and paleobiogeography. Part 1: Turonian. Carnets de Géologie 14, 211–252.
| Ostracodes from the Upper Cretaceous deposits of the Potiguar Basin, northeastern Brazil: taxonomy, paleoecology and paleobiogeography. Part 1: Turonian.Crossref | GoogleScholarGoogle Scholar |
Riutort, M., Álvarez-Presas, M., Lázaro, E., Solà, E., and Paps, J. (2012). Evolutionary history of the Tricladida and the Platyhelminthes: an up-to-date phylogenetic and systematic account. International Journal of Developmental Biology 56, 5–17.
| Evolutionary history of the Tricladida and the Platyhelminthes: an up-to-date phylogenetic and systematic account.Crossref | GoogleScholarGoogle Scholar |
Romeis, B. (1989). ‘Mikroskopische Technik.’ (Urban und Schwarzenberg: München, Germany.)
Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
| MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=7c842e23fc6c8622a464a3dbcf9c2662CAS |
Sluys, R. (1989). ‘A Monograph of the Marine Triclads.’ (Balkema: Rotterdam, The Netherlands).
Sluys, R. (1990). A monograph of the Dimarcusidae (Platyhelminthes, Seriata, Tricladida). Zoologica Scripta 19, 13–29.
| A monograph of the Dimarcusidae (Platyhelminthes, Seriata, Tricladida).Crossref | GoogleScholarGoogle Scholar |
Sluys, R., Kawakatsu, M., Riutort, M., and Baguñà, J. (2009). A new higher classification of planarian flatworms (Platyhelminthes, Tricladida). Journal of Natural History 43, 1763–1777.
| A new higher classification of planarian flatworms (Platyhelminthes, Tricladida).Crossref | GoogleScholarGoogle Scholar |
Sluys, R., Vila-Farré, M., Álvarez-Presas, M., Riutort, M., Kawakatsu, M., and Tulp, A. S. (2015). The diet and distribution of Pentacoelum kazukolinda (Kawakatsu and Mitchell, 1984), a maricolan planarian with a freshwater ecology. Zoologica Scripta 44, 72–91.
| The diet and distribution of Pentacoelum kazukolinda (Kawakatsu and Mitchell, 1984), a maricolan planarian with a freshwater ecology.Crossref | GoogleScholarGoogle Scholar |
Souza, S. T., Morais, A. L. N., Cordeiro, L. M., and Leal-Zanchet, A. M. (2015). The first troglobitic species of freshwater flatworm of the suborder Continenticola (Platyhelminthes) from South America. ZooKeys 470, 1–16.
| The first troglobitic species of freshwater flatworm of the suborder Continenticola (Platyhelminthes) from South America.Crossref | GoogleScholarGoogle Scholar |
Souza, S. T., Morais, A. L., Bichuette, M. E., and Leal-Zanchet, A. M. (2016). Two new species of freshwater flatworms (Platyhelminthes: Tricladida: Continenticola) from South American caves. Zootaxa 4092, 107–121.
| Two new species of freshwater flatworms (Platyhelminthes: Tricladida: Continenticola) from South American caves.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 | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=bf1c47d07b064fc1a91a82830ae5d513CAS |
Talavera, G., and Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.
| Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKrs7%2FP&md5=0dced01d514658b36c15b77c9c96df0fCAS |
Velho, N. M. R. C. (2011). Planárias límnicas (Tricladida: Dugesiidae) como modelos para experimentos de regeneração em ambientes de microgravidade e hipergravidade. PhD Thesis, Programa de Pós-Graduação em Biologia da Universidade do Vale do Rio dos Sinos, Brazil.
