Phylogenetic relationships within the flatworm genus Choeradoplana Graff (Platyhelminthes : Tricladida) inferred from molecular data with the description of two new sympatric species from Araucaria moist forests
V. S. Lemos A B C , G. P. Cauduro B , V. H. Valiati B C and A. M. Leal-Zanchet A C D
+ Author Affiliations
- Author Affiliations
A Instituto de Pesquisas de Planárias, Universidade do Vale do Rio dos Sinos – UNISINOS 93022-000, São Leopoldo, RS, Brazil.
B Laboratório de Biologia Molecular, Universidade do Vale do Rio dos Sinos – UNISINOS 93022-000, São Leopoldo, RS, Brazil.
C Programa de Pós-Graduação em Biologia, Universidade do Vale do Rio dos Sinos – UNISINOS 93022-000, São Leopoldo, RS, Brazil.
D Corresponding author. Email: zanchet@unisinos.br
Invertebrate Systematics 28(6) 605-627 https://doi.org/10.1071/IS14003
Submitted: 11 January 2014 Accepted: 7 September 2014 Published: 19 December 2014
Abstract
The genus Choeradoplana encompasses 11 species, nine of which have a restricted distribution and are only known from their type localities. Herein we describe two new species of Choeradoplana from Araucaria moist forests, C. minima, sp. nov. Lemos & Leal-Zanchet and C. benyai, sp. nov. Lemos & Leal-Zanchet, based on morphological and molecular data, and use two molecular markers to investigate their phylogenetic relationships with other species in the genus, including its type species. Both morphological and molecular analyses clearly distinguish C. minima, sp. nov., C. benyai, sp. nov. and C. iheringi. The analyses of the ITS-1, COI and sequence divergence data also indicated that C. benyai, sp. nov. is more closely related to the type species of the genus, C. iheringi, than to C. minima, sp. nov. The three species are sympatric in Araucaria moist forest areas of the São Francisco de Paula National Forest; C. minima, sp. nov. and C. benyai, sp. nov. seem to be endemic to their type localities. Regarding external morphology, C. benyai, sp. nov. and C. iheringi could be considered cryptic species, only distinguishable on the basis of the copulatory apparatus. However, immature specimens of C. benyai, sp. nov. and C. iheringi could only be identified based on molecular data. Our results demonstrate that COI should be used with caution for reconstructing phylogenies, and other slower-evolving nuclear genes are a feasible alternative for resolving some of the phylogenetic relationships.
Additional keywords: Atlantic Forest, Automatic Barcode Gap Discovery, COI, ITS-1, Geoplaninae, land flatworms, taxonomy, triclads.
References
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 |
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 | GoogleScholarGoogle Scholar | 21288273PubMed |
Amaral, V. S., Oliveira, S. M., and Leal-Zanchet, A. M. (2012). Three new species of land flatworms and comments on a complex of species in the genus Geoplana Stimpson (Platyhelminthes: Continenticola). Zootaxa 3338, 1–32.
Antunes, M. B., Marques, D. I. L., and Leal-Zanchet, A. M. (2008). Composição das comunidades de planárias terrestres (Platyhelminthes, Tricladida, Terricola) em duas áreas de floresta estacional decidual do sul do Brasil. Neotropical Biology and Conservation 31, 34–38.
| Composição das comunidades de planárias terrestres (Platyhelminthes, Tricladida, Terricola) em duas áreas de floresta estacional decidual do sul do Brasil.Crossref | GoogleScholarGoogle Scholar |
Antunes, M. B., Leal-Zanchet, A. M., and Fonseca, C. R. (2012). Habitat structure, soil properties, and food availability do not predict terrestrial flatworms occurrence in Araucaria Forest sites. Pedobiologia 55, 25–31.
| Habitat structure, soil properties, and food availability do not predict terrestrial flatworms occurrence in Araucaria Forest sites.Crossref | GoogleScholarGoogle Scholar |
Baguñà, J., Carranza, S., Pala, M., Ribera, C., Giribet, G., Arnedo, M., Ribas, M., and Riutort, M. (1999). From morphology and kariology to molecules. New methods for taxonomical identification of asexual populations of freshwater planarians. A tribute to Professor Mario Benazzi. The Italian Journal of Zoology 66, 207–214.
| From morphology and kariology to molecules. New methods for taxonomical identification of asexual populations of freshwater planarians. A tribute to Professor Mario Benazzi.Crossref | GoogleScholarGoogle Scholar |
Baptista, V. A., and Leal-Zanchet, A. M. (2005). Nova espécie de Geoplana Stimpson (Platyhelminthes, Tricladida, Terricola) do sul do Brasil. Revista Brasileira de Zoologia 22, 875–882.
| Nova espécie de Geoplana Stimpson (Platyhelminthes, Tricladida, Terricola) do sul do Brasil.Crossref | GoogleScholarGoogle Scholar |
Baptista, V. A., and Leal-Zanchet, A. M. (2010). Land flatworm community structure in a subtropical deciduous forest in Southern Brazil. Belgian Journal of Zoology 140, 83–90.
Carbayo, F., and Froehlich, E. M. (2012). Three new Brazilian species of the land planarian Choeradoplana (Platyhelminthes: Tricladida: Geoplaninae), and an emendation of the genus. Journal of Natural History 46, 1153–1177.
| Three new Brazilian species of the land planarian Choeradoplana (Platyhelminthes: Tricladida: Geoplaninae), and an emendation of the genus.Crossref | GoogleScholarGoogle Scholar |
Carbayo, F., and Leal-Zanchet, A. M. (2001). A new species of terrestrial planarian (Platyhelminthes, Tricladida, Terrestrial) from South Brazil. Brazilian Journal of Biology 61, 437–447.
| A new species of terrestrial planarian (Platyhelminthes, Tricladida, Terrestrial) from South Brazil.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnltlGlsA%3D%3D&md5=a87c083829bf01dd157b7b3895065d9fCAS |
Carbayo, F., and Leal-Zanchet, A. M. (2003). Two new genera of geoplaninid land planarians (Platyhelminthes: Tricladida: Terricola) of Brazil in the light of cephalic specialisations. Invertebrate Systematics 17, 449–468.
| Two new genera of geoplaninid land planarians (Platyhelminthes: Tricladida: Terricola) of Brazil in the light of cephalic specialisations.Crossref | GoogleScholarGoogle Scholar |
Carbayo, F., Leal-Zanchet, A. M., and Vieira, E. M. (2002). Flatworms (Platyhelminthes, Tricladida, Terricola) diversity versus man-induced disturbance in ombrophilous rainforest from Southern Brazil. Biodiversity and Conservation 11, 1091–1104.
| Flatworms (Platyhelminthes, Tricladida, Terricola) diversity versus man-induced disturbance in ombrophilous rainforest from Southern Brazil.Crossref | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar |
Carranza, S., Littlewood, D. T. J., Clough, K. A., Ruiz, I., Baguñà, J., and Riutort, M. (1998). A robust molecular phylogeny of the Tricladida (Platyhelminthes, Seriata) and a reassessment of morphological synapomorphies. Proceedings. Biological Sciences 265, 631–640.
| A robust molecular phylogeny of the Tricladida (Platyhelminthes, Seriata) and a reassessment of morphological synapomorphies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M%2FpvVWntw%3D%3D&md5=8228906b3e48352f83546093d6ce4ee4CAS |
Castro, R. A., and Leal-Zanchet, A. M. (2005). Composição de comunidades de planárias terrestres (Platyhelminthes) em áreas de Floresta Estacional Decidual e de Campo na região central do Rio Grande do Sul, Brasil. Acta Biologica Leopoldensia 27, 147–150.
Du Bois-Reymond Marcus, E. (1951). On south american geoplanids. Boletim da Faculdade de Filosofia Ciências e Letras da Universidade de São Paulo, série Zoologia 16, 217–255.
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–793.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Fonseca, C. R., Ganade, G., Baldissera, R., Becker, C. G., Boelter, C. R., Brescovit, A. D., Campos, L. M., Fleck, T., Fonseca, V. S., Hartz, S. M., Joner, F., Kaffer, M. I., Leal-Zanchet, A. M., Marcelli, M. P., Mesquita, A. S., Mondin, C. A., Paz, C. P., Petry, M. V., Piovensan, S. M., Putzke, J., Stranz, A., Vergara, M., and Vieira, E. M. (2009). Towards an ecologically sustainable forestry in the Atlantic Forest. Biological Conservation 142, 1209–1219.
| Towards an ecologically sustainable forestry in the Atlantic Forest.Crossref | GoogleScholarGoogle Scholar |
Froehlich, C. G. (1955a). On the biology of land planarians. Boletim da Faculdade de Filosofia Ciências e Letras da Universidade de São Paulo, série Zoologia 20, 263–272.
Froehlich, C. G. (1955b). Sobre a Morfologia e Taxonomia das Geoplanidae. Boletim da Faculdade de Filosofia, Ciências e Letras. Série Zoologia 19, 195–279.
Froehlich, C. G. (1959). On Geoplanids from Brazil. Boletim da Faculdade de Filosofia, Ciências e Letras. Série Zoologia. 22, 201–242.
Froehlich, E. M., and Leal-Zanchet, A. M. (2003). A new species of terrestrial planarian of the genus Notogynaphallia Ogren & Kawakatsu (Platyhelminthes, Tricladida, Terricola) from south Brazil and some comments on the genus. Revista Brasileira de Zoologia 20, 745–753.
| A new species of terrestrial planarian of the genus Notogynaphallia Ogren & Kawakatsu (Platyhelminthes, Tricladida, Terricola) from south Brazil and some comments on the genus.Crossref | GoogleScholarGoogle Scholar |
Graff, L. V. (1896). Über das System und die geographische Verbreitung der Landplanarien. Verhandlungen der deutschen zoologischen Gesellschaft 6, 61–75.
Graff, L. V. (1899). ‘Monographie der Turbellarien: II. Tricladida Terricola.’ (Engelmann, Leipzig, Germany.)
Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
| A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 14530136PubMed |
Hall, T. A. (1999). BioEdit: a user-friendly biological sequences alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
| 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D&md5=6aaad10f45ced27e84f44de743042b56CAS |
Hasegawa, M., Kishino, H., and Yano, T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.
| Dating of the human-ape splitting by a molecular clock of mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXmtFSns7g%3D&md5=392aa8dad9eb52877dd6b829ebf712dbCAS | 3934395PubMed |
Jones, H. D., and Cumming, M. S. (1998). Feeding behaviour of the termite-eating planarian Microplana termitophaga (Platyhelminthes: Turbellaria: Tricladida: Terricola) in Zimbabwe. Journal of Zoology 245, 53–64.
| Feeding behaviour of the termite-eating planarian Microplana termitophaga (Platyhelminthes: Turbellaria: Tricladida: Terricola) in Zimbabwe.Crossref | GoogleScholarGoogle Scholar |
Katoh, K., and Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9, 286–298.
| Recent developments in the MAFFT multiple sequence alignment program.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpt1artrs%3D&md5=d3f40cfe601202676deea9a82d9894d7CAS | 18372315PubMed |
Kawaguti, S. (1932). On the physiology of land planarians. III. The problems of desiccation. Memoirs of the Faculty of Science and Agriculture 7, 39–55.
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitution through comparative studies of nucleotide sequences. Evolution 16, 111–120.
| A simple method for estimating evolutionary rates of base substitution through comparative studies of nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXmtFSktg%3D%3D&md5=c33259eaaa0aa145bad4101bf68dca77CAS |
Lázaro, E. M., Sluys, R., Pala, M., Stocchino, G. A., 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, A. M., and Baptista, V. A. (2009). Planárias terrestres (Platyhelminthes: Tricladida) em áreas de floresta com araucária no Rio Grande do Sul. In ‘Floresta com Araucária: Ecologia, Conservação e Desenvolvimento Sustentável.’ (Eds C. R. S. Fonseca, A. F. Souza, T. L. Dutra, A. M. Leal-Zanchet, A. Backes and G. M. S. Ganade) pp. 199–207. (Holos, Ribeirão Preto, Brazil).
Leal-Zanchet, A. M., and Carbayo, F. (2000). Fauna de planárias terrestres (Platyhelminthes, Tricladida, Terricola) da Floresta Nacional de São Francisco de Paula, RS, Brasil: Uma análise preliminar. Acta Biologica Leopoldensia 22, 19–25.
Leal-Zanchet, A. M., and Carbayo, F. (2001). Two new species of Geoplanidae (Platyhelminthes, Tricladida, Terricola) of South Brazil. Journal of Zoology 253, 433–446.
| Two new species of Geoplanidae (Platyhelminthes, Tricladida, Terricola) of South Brazil.Crossref | GoogleScholarGoogle Scholar |
Leal-Zanchet, A. M., and Souza, S. A. (2003). Redescrição de Choeradoplana iheringi Graff (Platyhelminthes, Tricladida, Terricola). Revista Brasileira de Zoologia 20, 523–530.
| Redescrição de Choeradoplana iheringi Graff (Platyhelminthes, Tricladida, Terricola).Crossref | GoogleScholarGoogle Scholar |
Leal-Zanchet, A. M., Baptista, V., Campos, L. M., and Raffo, J. F. (2011). Spatial and temporal patterns of land flatworms assemblages in Brazilian Araucaria forests. Invertebrate Biology 130, 25–33.
| Spatial and temporal patterns of land flatworms assemblages in Brazilian Araucaria forests.Crossref | GoogleScholarGoogle Scholar |
Leal-Zanchet, A. M., Rossi, I., Seitenfus, A. L. R., and Alvarenga, J. (2012). Two new species of land flatworms and comments on the genus Pasipha Ogren & Kawakatsu, 1990 (Platyhelminthes: Continenticola). Zootaxa 3583, 1–21.
Lemos, V. S., and Leal-Zanchet, A. M. (2008). Two new species of Notogynaphallia Ogren & Kawakatsu (Platyhelminthes: Tricladida: Terricola) from Southern Brazil. Zootaxa 1907, 28–46.
Marcus, E. (1951). Turbellaria brasileiros (9). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo. Série Zoologia 16, 1–217.
Negrete, L., and Brusa, F. (2012). Choeradoplana crassiphalla sp. nov. (Platyhelminthes: Tricladida: Geoplanidae): a new species of land planarian from the Atlantic Forest of Argentina. Studies on Neotropical Fauna and Environment 47, 227–237.
| Choeradoplana crassiphalla sp. nov. (Platyhelminthes: Tricladida: Geoplanidae): a new species of land planarian from the Atlantic Forest of Argentina.Crossref | GoogleScholarGoogle Scholar |
Ogren, R. E. (1995). Predation behaviour of land planarians. Hydrobiologia 305, 105–111.
| Predation behaviour of land planarians.Crossref | GoogleScholarGoogle Scholar |
Ogren, R. E., and Kawakatsu, M. (1990). Index to the species of the family Geoplanidae (Turbellaria, Tricladida, Terricola) Part I: Geoplaninae. Bulletin of the Fuji Women’s College. Ser. II 28, 79–166.
Oliveira, S. M., Boll, P. K., Baptista, V. A., and Leal-Zanchet, A. M. (2014). Effects of pine invasion on land planarian communities in an area covered by Araucaria moist forest. Zoological Studies 53, 19.
| Effects of pine invasion on land planarian communities in an area covered by Araucaria moist forest.Crossref | GoogleScholarGoogle Scholar |
Posada, D., and Crandall, K. A. (1998). Modeltest: Testing the model of DNA substitution. Bioinformatics 14, 817–818.
| Modeltest: Testing the model of DNA substitution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktlCltw%3D%3D&md5=787c5224a9b3b4a919b481f4db32fc35CAS | 9918953PubMed |
Prasniski, M. E. T., and Leal-Zanchet, A. M. (2009). Predatory behavior of the land flatworm Notogynaphallia abundans (Platyhelminthes: Tricladida). Zoologia 26, 606–612.
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 | 1:STN:280:DC%2BC38zlsFeltQ%3D%3D&md5=6a988792b76cb4958ac97b6ceacba539CAS | 21883587PubMed |
Rodríguez, F. J., Oliver, J. L., Marín, A., and Medina, J. R. (1990). The general stochastic model of nucleotide substitution. Journal of Theoretical Biology 142, 485–501.
| The general stochastic model of nucleotide substitution.Crossref | GoogleScholarGoogle Scholar |
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=d5b84f5cc16cfb75b367ced57a76cb2cCAS | 12912839PubMed |
Sluys, R. (1989). ‘A Monograph of the Marine Triclads.’ (A. A. Balkema: Rotterdam, The Netherlands.)
Sluys, R. (1995). Platyhelminthes as paleogeographical indicators. Hydrobiologia 305, 49–53.
| Platyhelminthes as paleogeographical indicators.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 |
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=0c5c46451d549b55ffe3d65d7213c7a5CAS | 17654362PubMed |
Winsor, L. (2006). New and revised terrestrial flatworm taxa (Platyhelminthes: Tricladida: Terricola) of Australia and the Subantarctic Islands of New Zealand. Tuhinga: Records of the Museum of New Zealand Te Papa Tongarewa 17, 81–104.
Winsor, L. (2009). A new subfamily, new genus and new species of terrestrial flatworm (Platyhelminthes: Tricladida: Geoplanidae) from Stewart Island, New Zealand. Tuhinga: Records of the Museum of New Zealand Te Papa Tongarewa 20, 23–32.
Winsor, L., Johns, P. M., and Yeates, G. W. (1998). Introduction, and ecological and systematic background, to the Terricola (Tricladida). Pedobiologia 42, 389–404.
Xia, X., and Xie, Z. (2001). DAMBE: Software package for data analysis in molecular biology and evolution. The Journal of Heredity 92, 371–373.
| DAMBE: Software package for data analysis in molecular biology and evolution.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvptlagtA%3D%3D&md5=41f1962fe72fbb78474aba16da54e696CAS | 11535656PubMed |
