Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Species richness in the genus Microplana (Platyhelminthes, Tricladida, Microplaninae) in Europe: as yet no asymptote in sight

Eduardo Mateos A , Ronald Sluys B D , Marta Riutort C and Marta Álvarez-Presas C
+ Author Affiliations
- Author Affiliations

A Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal 643, 08028 Barcelona, Spain.

B Naturalis Biodiversity Center, PO Box 9517, 2300 RA Leiden, The Netherlands.

C Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Av. Diagonal 643, 08028 Barcelona, Spain.

D Corresponding author. Email: Ronald.Sluys@naturalis.nl

Invertebrate Systematics 31(3) 269-301 https://doi.org/10.1071/IS16038
Submitted: 25 April 2016  Accepted: 1 December 2016   Published: 9 May 2017

Abstract

This study forms a major step towards a comprehensive morphological and molecular analysis of the species diversity of European microplanid land planarians. It presents a molecular phylogenetic tree on the basis of information from the genes Cox1, 18S, 28S and elongation factor 1-α, and applies molecular and morphological species delimitation methodologies for Microplana specimens sampled over a wide geographic range within Europe. The study suggests that as yet there is no plateau or asymptote in the accumulation curve for European Microplana species, as our results facilitated an integrative delimitation of seven new species as well as the diagnosis of new populations of three already known species and one doubtful or problematic species. In some cases, the new records considerably enlarged the known range of a species. An integrative account is provided of each of these species. Molecular sequence information on newly collected land flatworms may quickly point the planarian systematist to taxa that need to be examined morphologically and thus may considerably reduce laborious and time-consuming histological analyses.

Additional keywords: biodiversity, BP&P, Continenticola, GMYC, integrative taxonomy, molecular systematics, taxonomic inflation.


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 |

Álvarez-Presas, M., Carbayo, F., Rozas, J., and Riutort, M. (2011). Land planarians (Platyhelminthes) as a model organism for fine-scale 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 fine-scale phylogeographic studies: understanding patterns of biodiversity in the Brazilian Atlantic Forest hotspot.CrossRef |

Ball, I. R., and Sluys, R. (1990). Turbellaria: Tricladida: Terricola. In ‘Soil Biology Guide’. (Ed. D. L. Dindal.) pp. 137–153. (John Wiley & Sons: New York, NY.)

Bendl, W. E. (1908). Beiträge zur Kenntnis des Genus Rhynchodemus. Zeitschrift für Wissenschaftliche Zoologie 89, 525–554.

Bendl, W. E. (1909a). Europäische Rhynchodemiden I. Zeitschrift fur Wissenschartliche Zoologie 92, 51–74.

Bendl, W. E. (1909b). Der ‘Ductus genito-intestinalis’ der Plathelminthen. Zoologischer Anzeiger 34, 294–299.

Bickford, D., Lohman, D., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K., and Das, I. (2007). Cryptic species: a new window on diversity and conservation. Trends in Ecology 22, 148–155.
Cryptic species: a new window on diversity and conservation.CrossRef |

Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C. H., Xie, D., Suchard, M., Rambaut, A., and Drummond, A. (2014). BEAST2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.
BEAST2: a software platform for Bayesian evolutionary analysis.CrossRef |

Caley, M. J., Fisher, R., and Mengersen, K. (2014). Global species richness estimates have not converged. Trends in Ecology & Evolution 29, 187–188.
Global species richness estimates have not converged.CrossRef |

Carbayo, F., Álvarez-Presas, M., Olivares, C. T., Marques, F. P. L., Froehlich, E. M., 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 |

Costello, M. J., Wilson, S., and Houlding, B. (2012). Predicting total global species richness using rates of species description and estimates of taxonomic effort. Systematic Biology 61, 871–883.
Predicting total global species richness using rates of species description and estimates of taxonomic effort.CrossRef |

Costello, M. J., Wilson, S., and Houlding, B. (2013). More taxonomists describing significantly fewer species per unit effort may indicate that most species have been discovered. Systematic Biology 62, 616–624.
More taxonomists describing significantly fewer species per unit effort may indicate that most species have been discovered.CrossRef |

Cracraft, J. (1983). Species concepts and speciation analysis. Current Ornithology 1, 159–187.
Species concepts and speciation analysis.CrossRef |

Cracraft, J. (1987). Species concepts and the ontology of evolution. Biology & Philosophy 2, 329–346.
Species concepts and the ontology of evolution.CrossRef |

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 | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=1e151a811e335310e17f8244e6b6ccbaCAS |

De Beauchamp, P. (1913). Planaires des broméliacées de Costa-Rica recueillies par Mr. C. Picado. Archives de Zoologie Expérimentale et Générale 51, 41–52.

De Beauchamp, P. (1936). Turbellariés et Bryozoaires. Mission Scientifique de l’Omo III(23), 141–153.

de Queiroz, K. (1998). The general lineage concept of species, species criteria, and the process of speciation – a conceptual unification and terminological recommendations. In ‘Endless Forms – Species and Speciation’. (Eds D. J. Howard and S. H. Berlocher.) pp. 57–75. (Oxford University Press: Oxford, UK.)

de Queiroz, K. (1999). The general lineage concept of species and the defining properties of the species category. In ‘Species – New Interdisciplinary Essays’. (Ed. R. A. Wilson.). pp. 49–89. (MIT Press: Cambridge, MA.).

de Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology 56, 879–886.
Species concepts and species delimitation.CrossRef |

Drummond, A. J., and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
BEAST: Bayesian evolutionary analysis by sampling trees.CrossRef |

Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.CrossRef | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=1128fe2c54a768f2b18bd3a1ecbe3c88CAS |

Du Bois-Reymond Marcus, E. (1957). On Turbellaria. Anais da Academia Brasileira de Ciencias 29, 153–191.

Essl, F., Rabitsch, W., Dullinger, S., Moser, D., and Milasowszky, N. (2013). How well do we know species richness in a well-known continent? Temporal patterns of endemic and widespread species descriptions in the European fauna. Global Ecology and Biogeography 22, 29–39.
How well do we know species richness in a well-known continent? Temporal patterns of endemic and widespread species descriptions in the European fauna.CrossRef |

Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
Confidence limits on phylogenies: an approach using the bootstrap.CrossRef |

Fontaine, B., van Achterberg, K., Alonso-Zarazaga, M. A., Araujo, R., Asche, M., Aspöck, H., Aspöck, U., Audisio, P., Aukema, B., Bailly, N., Balsamo, M., Bank, R. A., Belfiore, C., Bogdanowicz, W., Boxshall, G., Burckhardt, D., Chylarecki, P., Deharveng, L., Dubois, A., Enghoff, H., Fochetti, R., Fontaine, C., Gargominy, O., Soledad Gomez Lopez, M., Goujet, D., Harvey, M. S., Heller, K.-G., van Helsdingen, P., Hoch, H., De Jong, Y., Karsholt, O., Los, W., Magowski, W., Massard, J. A., McInnes, S. J., Mendes, L. F., Mey, E., Michelsen, V., Minelli, A., Nieto Nafrıa, J. M., van Nieukerken, E. J., Pape, T., De Prins, W., Ramos, M., Ricci, C., Roselaar, C., Rota, E., Segers, H., Timm, T., van Tol, J., and Bouchet, P. (2012). New species in the Old World: Europe as a frontier in biodiversity exploration, a test bed for 21st century taxonomy. PLoS One 7, e36881.
New species in the Old World: Europe as a frontier in biodiversity exploration, a test bed for 21st century taxonomy.CrossRef | 1:CAS:528:DC%2BC38XotVyqsr8%3D&md5=6fedb5ea7b6fb67e32e51f4262e918e6CAS |

Fujisawa, T., and Barraclough, T. G. (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.
Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets.CrossRef |

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=01675b96feb07335d6568390e1c23744CAS |

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

Hyman, L. H. (1954). Some land planarians of the United States, with remarks on nomenclature. American Museum Novitates 1667, 1–21.

Jones, H. D., Webster, B. L., Littlewood, D. T. J., and McDonald, J. C. (2008). Molecular and morphological evidence for two new species of terrestrial planarians of the genus Microplana (Platyhelminthes; Turbellaria; Tricladida; Terricola) from Europe. Zootaxa 1945, 1–38.

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 | 1:CAS:528:DC%2BC3sXksFWisLc%3D&md5=9b63ef51572a7695e00dde761602e188CAS |

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., Meintjes, 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 |

Kuhner, M. K. (2006). LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22, 768–770.
LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters.CrossRef | 1:CAS:528:DC%2BD28Xit1Ont7k%3D&md5=290dcc2928b99d65219d746ba1b7ea7bCAS |

Leaché, A. D., and Fujita, M. K. (2010). Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proceedings of the Royal Society B 277, 3071–3077.
Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus).CrossRef |

Lohse, K. (2009). Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006). Systematic Biology 58, 439–442.
Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006).CrossRef |

Meixner, J. (1921). Rhynchodemus peneckei n. sp., ein Landtriclade aus Steiermark. Zoologische Jahrbücher. Abteilung für Systematik 44, 355–374.

Minelli, A. (1976). Planari terrestri dell’Arcipelago Toscano. Biogeografia 5, 93–98.
Planari terrestri dell’Arcipelago Toscano.CrossRef |

Minelli, A. (1977). A taxonomic review of the terrestrial planarians of Europe. Bollettino di Zoologia 44, 399–419.
A taxonomic review of the terrestrial planarians of Europe.CrossRef |

Ogren, R. E. (1984). The land planarian Microplana terrestris (Platyhelminthes: Turbellaria) from the United States. Transactions of the American Microscopical Society 103, 130–136.
The land planarian Microplana terrestris (Platyhelminthes: Turbellaria) from the United States.CrossRef |

Ogren, R. E. (1986). Development of the reproductive apparatus of the land planarian Rhynchodemus sylvaticus (Turbellaria: Tricladida) and its significance for classification in the genus. Hydrobiologia 132, 175–180.
Development of the reproductive apparatus of the land planarian Rhynchodemus sylvaticus (Turbellaria: Tricladida) and its significance for classification in the genus.CrossRef |

Ogren, R. E. (1988). Developmental and morphological evidence that the land planarians Microplana terrestris and M. atrocyanea are conspecific. Fortschritte der Zoologie 36, 395–398.

Padial, J. M., Miralles, A., de la Riva, I., and Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology 7, 16.
The integrative future of taxonomy.CrossRef |

Papadopoulou, A., Monaghan, M. T., Barraclough, T. G., and Vogler, A. P. (2009). Sampling error does not invalidate the Yule-coalescent model for species delimitation. A response to Lohse (2009). Systematic Biology 58, 442–444.
Sampling error does not invalidate the Yule-coalescent model for species delimitation. A response to Lohse (2009).CrossRef |

Pons, J., Barraclough, T. G., Gomez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., Kamoun, S., Sumlin, W. D., and Vogler, A. P. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.
Sequence-based species delimitation for the DNA taxonomy of undescribed insects.CrossRef |

Rambaut, A., Suchard, M., Xie, D., and Drummond, A. (2014). Tracer v1.6. Available at http://beast.bio.ed.ac.uk/Tracer [Verified 17 February 2017].

Rannala, B., and Yang, Z. (2003). Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164, 1645–1656.
| 1:CAS:528:DC%2BD3sXnvF2nt74%3D&md5=57e592a2f41bca24d8eab6d009b25268CAS |

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 |

Saint-Hilaire, C. (1910). Beobachtungen über die intrazelluläre verdauung in den darmzellen der planarien. Zeitschrift für Allgemeine Physiologie 11, 177–248.

Sangster, G., and Luksenburg, J. A. (2015). Declining rates of species described per taxonomist: slowdown of progress or a side-effect of improved quality of taxonomy? Systematic Biology 64, 144–151.
Declining rates of species described per taxonomist: slowdown of progress or a side-effect of improved quality of taxonomy?CrossRef |

Schlick-Steiner, B. C., Steiner, F. M., Seifert, B., Stauffer, C., Christian, E., and Crozier, R. H. (2010). Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology 55, 421–438.
Integrative taxonomy: a multisource approach to exploring biodiversity.CrossRef | 1:CAS:528:DC%2BC3cXptVShtQ%3D%3D&md5=bd48b7260df87fe6c1a49a7f9f380984CAS |

Sket, B., Paragamian, K., and Trontelj, P. (2004). A census of the obligate subterranean fauna of the Balkan Peninsula. In ‘Balkan Biodiversity’. (Eds H. I. Griffiths, B. Kryštufek and J. M. Reed.) pp. 309–322. (Kluwer Academic Publishers: Dordrecht, The Netherlands.)

Sluys, R. (1989). Phylogenetic relationships of the triclads (Platyhelminthes, Seriata, Tricladida). Bijdragen tot de Dierkunde 59, 3–25.

Sluys, R. (1991). Species concepts, process analysis, and the hierarchy of nature. Experientia 47, 1162–1170.
Species concepts, process analysis, and the hierarchy of nature.CrossRef |

Sluys, R. (2013). The unappreciated, fundamentally analytical nature of taxonomy and the implications for the inventory of biodiversity. Biodiversity and Conservation 22, 1095–1105.
The unappreciated, fundamentally analytical nature of taxonomy and the implications for the inventory of biodiversity.CrossRef |

Sluys, R., and Riutort, M. (in prep.). Planarian diversity and phylogeny. In ‘The Pplanarian Mmodel Ssystem – Methods and Protocols’. (Ed. J. Rink.) (Springer: Heidelberg, Germany.)

Sluys, R., Mateos, E., Riutort, M., and Álvarez-Presas, M. (2016). Towards a comprehensive, integrative analysis of the diversity of European microplaninid land flatworms (Platyhelminthes, Tricladida, Microplaninae), with the description of two peculiar new species. Systematics and Biodiversity 14, 9–31.
Towards a comprehensive, integrative analysis of the diversity of European microplaninid land flatworms (Platyhelminthes, Tricladida, Microplaninae), with the description of two peculiar new species.CrossRef |

Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.CrossRef | 1:CAS:528:DC%2BC2cXmvFCjsbc%3D&md5=dbe02a1b9e110b233409dd1d5b71d108CAS |

Steinböck, O. (1924). Untersuchungen über die Geschlechtstrakt-Darmverbindung bei Turbellarien nebst einem Beitrag zur Morphologie des Trikladendarmes. Zeitschrift fur Morphologie und Oekologie der Tiere 2, 461–504.
Untersuchungen über die Geschlechtstrakt-Darmverbindung bei Turbellarien nebst einem Beitrag zur Morphologie des Trikladendarmes.CrossRef |

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 | 1:CAS:528:DC%2BD2sXhtFKrs7%2FP&md5=0047ba3b5231ef0904a5c2560f64ab2cCAS |

Vila-Farré, M., Mateos, E., Sluys, R., and Romero, R. (2008). Terrestrial planarians (Platyhelminthes, Tricladida, Terricola) from the Iberian Peninsula: new records and description of three new species. Zootaxa 1739, 1–20.

Vila-Farré, M., Sluys, R., Mateos, E., Jones, H. D., 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 |

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, Germany.)

Von Kennel, J. (1882). Die in Deutschland gefundenen landplanarien Rhynchodemus terrestris O. F. Müller und Geodesmus bilineatus Mecznikoff. Arbeiten aus dem Zoologisch-Zootomischen Institut in Wurzburg 5, 120–160.

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

Winsor, L., and Sluys, R. (in prep.). Basic histological techniques for planarians. In ‘The Planarian Model System – Methods and Protocols’. (Ed. J. Rink.) (Springer: Heidelberg, Germany.)

Winsor, L., and Stevens, M. (2005). Terrestrial flatworms (Platyhelminthes: Tricladida: Terricola) from sub-Antarctic Macquarie Island. Kanunnah 1, 17–32.

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 | 1:CAS:528:DC%2BC3cXmslGrtLs%3D&md5=475bb94407ce8052350bbc7527e0cfa2CAS |

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 | 1:CAS:528:DC%2BC2MXisFaktL4%3D&md5=3a1ee11ea28563988ca1a6847fd70f4aCAS |

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 | 1:CAS:528:DC%2BC3sXhslWnsbzL&md5=590879895fbb6dbd45bc489e44a35593CAS |



Rent Article (via Deepdyve) Supplementary MaterialSupplementary Material (2.6 MB) Export Citation

View Altmetrics