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Rolling Into the Deep of the Land Planarian Genus Choeradoplana (Tricladida, Continenticola, Geoplanidae) Taxonomy

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Rolling Into the Deep of the Land Planarian Genus Choeradoplana (Tricladida, Continenticola, Geoplanidae) Taxonomy Org Divers Evol (2018) 18:187–210 https://doi.org/10.1007/s13127-017-0352-4 ORIGINAL ARTICLE Rolling into the deep of the land planarian genus Choeradoplana (Tricladida, Continenticola, Geoplanidae) taxonomy Fernando Carbayo1 & Marcos Santos Silva1 & Marta Riutort2 & Marta Álvarez-Presas2 Received: 27 June 2017 /Accepted: 1 November 2017 /Published online: 1 December 2017 # Gesellschaft für Biologische Systematik 2017 Abstract The land planarian genus Choeradoplana present a comprehensive phylogenetic tree including most (Plathelminthes, Tricladida) is currently integrated by 13 spe- Choeradoplana species. The tree, well supported, allows mak- cies. In previous works, morphological variation in its type ing some preliminary inferences on the evolution of the group species, Choeradoplana iheringi, was reported, but no attempt and its historical biogeography. to test whether it is just a single species has been made yet. In order to disentangle the taxonomy of this species and further Keywords ABGD . bPTP . BP&P . Cryptic species . members of the genus, we sampled new specimens and com- Flatworms . GMYC . Histology . Geoplaninae bined morphological and molecular data and also have evalu- ated the performance of diverse methods of molecular species delimitation. Our data point to the presence of two cryptic spe- Introduction cies named C. iheringi, plus two new species, all hidden under the same general appearance. An in-depth morphological study In recent years, the use of molecular data has increased con- of the specimens allowed detection of diagnostic morphologi- siderably the discovery of cryptic species (considering cryptic cal traits in each species, for which we also propose a molecular species those morphologically indistinguishable but diagnosis. This integrative taxonomic study demonstrates once belonging to different evolutionary lineages; Waeschenbach again the usefulness of molecular tools to weigh minor mor- et al. 2012) and promoted their study (Bickford et al. 2007). phological characteristics and thus reveal the existence of spe- This increase is related to the need of a better knowledge of cies that would otherwise remain cryptic. However, under cer- species diversity in order to design good conservation plans tain parameters, the molecular methods may over-split species for endangered regions or for the control of invasive species, with a high genetic structure, maybe pointing to incipient spe- among other causes. For instance, if we are only aware of the ciation. This makes critical the use of these methods combined species at the morphotype level, we may be underestimating with a comprehensive morphological approach. We also the real biodiversity both at the taxonomic and genetic levels, which is important for the study of potential distribution Electronic supplementary material The online version of this article changes underwent by species as a result of climate change (https://doi.org/10.1007/s13127-017-0352-4) contains supplementary (Bálint et al. 2011). Generally, the use of the DNA barcoding material, which is available to authorized users. initiative (Hebert et al. 2003), based on a single short fragment of DNA, is sufficient to identify the species or even delimit * Marta Álvarez-Presas new ones, but in many cases, the use of other tools (more [email protected] morphological characters, more genes, or new molecular tools to delimit species) is necessary to the determination of evolu- 1 Laboratório de Ecologia e Evolução, Escola de Artes, Ciências e Humanidades, Universidade de São Paulo (USP), Av. Arlindo Bettio, tionary divergent taxonomic units (Prévot et al. 2013; 1000, CEP, São Paulo, SP 03828-000, Brazil Hamilton et al. 2014). 2 Departament de Genètica, Microbiologia i Estadística, Facultat de For terrestrial planarians (Platyhelminthes, Tricladida, Biologia and Institut de Recerca de la Biodiversitat (IRBio), Continenticola, Geoplanidae), repeated cases of cryptic spe- Universitat de Barcelona, Av Diagonal, 643 08028 Barcelona, Spain cies have been detected (Lemos et al. 2014; Álvarez-Presas 188 Carbayo F. et al. et al. 2015; Carbayo et al. 2016; Mateos et al. 2017). Thanks Previous studies that include this species already showed to the combination of different methodologies of molecular signs of the presence of cryptic species confounded under the species delimitation (GMYC and BP&P for instance) it has name C. iheringi. Riester (1938) and Leal-Zanchet and de been possible to focus efforts on the morphological character- Souza (2003) documented morphological variation in ization of molecularly differentiated lineages that until then C. iheringi mainly regarding the relative size of parts of the had been considered the same species, in an integrative tax- copulatory apparatus. This variation was interpreted as a result onomy approach. Thus, it has shown profitable for the taxon- of artifactual contraction, physiological condition, or popula- omy of this group the application of a protocol beginning with tional variation (Riester 1938; Leal-Zanchet and de Souza an external morphology assignation to morphospecies, subse- 2003). quent molecular testing of the morphospecies, and, when both More recently, Carbayo et al. (2013) provided a molecular approaches are not congruent, deeper morphological exami- phylogeny of the subfamily Geoplaninae, into which two nation (Álvarez-Presas et al. 2015; Carbayo et al. 2016; specimens of C.cf.iheringi were represented. One specimen Mateos et al. 2017). was collected in São Francisco de Paula, and another in the Geoplanids of the genus Choeradoplana Graff, 1896 are Serra da Bocaina National Park (SP), close to Salesópolis. generally easy to recognize by means of their characteristical- They noted the paraphyletic status of the species and sug- ly rolled-up and laterally expanded cephalic end. A peculiar gested that morphological differences, already highlighted characteristic of the representatives of this genus is the pres- by Leal-Zanchet and de Souza (2003), might be indicating ence of a very strong longitudinal muscular subepidermic lay- non-conspecificity. er that allows them, in an alarm state, to escape by curling Here, we present a comprehensive molecular phylogenetic upward the back end and roll forward until they touch the framework of 11 species of the genus, including numerous substrate again, resulting in a sort of somersault (Froehlich representatives of Choeradoplana cf. iheringi, to test the phy- 1955a). letic status of this species. The representativeness of the genus The genus is currently integrated by 13 species, all of them also encompasses two new cryptic species which can be con- with neotropical distribution (found in Brazil and Argentina). fused with C. iheringi as regards of the chromatic pattern of Most species of Choeradoplana have been described and their dorsum. Finally, robustness of our phylogenetic trees delimited by means of morphological traits only. Molecular also allowed us to make considerations on the biogeography approaches to the taxonomy of the genus were briefly ad- of the genus. dressed by Carbayo et al. (2013). They suggested a polyphy- letic status for C. iheringi Graff, 1899 (Carbayo et al. 2013). More recently, C. minima Lemos & Leal-Zanchet, 2014 and Material and methods C. benyai Lemos & Leal-Zanchet, 2014 (Lemos et al. 2014) were described based on morphological and molecular data Morphological analyses (Lemos et al. 2014). No further taxonomic molecular works have been issued. We examined the type material of C. iheringi, and most spec- Morphological aspects of species of the genus are unevenly imens studied by Riester (1938), Marcus (1951), Froehlich studied, ranging from C. ehrenreichi Graff, 1899—the internal (1955b), and Leal-Zanchet and de Souza (2003) and further organs of which are unknown—to Choeradoplana iheringi, individuals collected recently by us. Graff’s material consists the type species of the genus, which was studied by several of sagittal and transverse sections of six cephalic portions, authorities. This species was originally described from several sagittal sections of a pharynx, sagittal sections of a copulatory specimens collected in Taquara (State of Rio Grande do Sul apparatus, and sagittal-to-horizontal sections of a twisted por- (RS)) (Fig. 1)(Graff1899). Riester (1938) studied additional tion of the body that includes pharynx and copulatory appa- material collected in Gorduras (State of Minas Gerais (MG)), ratus. We reconstructed the copulatory apparatus of the spec- Teresópolis (State of Rio de Janeiro (RJ)), and Riberião Pires imen described and illustrated by Graff (1899, Fig. 45, p. 194). (State of São Paulo (SP)). From the latter locality, Marcus Riester’s material consists of several specimens having (1951) and Froehlich (1955b) examined further specimens. some parts of their bodies preserved in balsam and other parts Froehlich (1956) also reported more specimens from sectioned on histological slides. We took microphotographs of Teresópolis bearing a chromatic pattern of the dorsum similar the four copulatory apparatuses available and analyzed them. to that described in Riester (1938). Leal-Zanchet and de Souza The copulatory apparatus of the specimens N653 and N83 do (2003) redescribed the species by examining individuals from not match the general anatomy of the nominal C. iheringi and São Francisco de Paula (RS) and Salesópolis (SP). Regarding were not further considered here. their ecology, the species prefers altered habitats so that they Marcus’ material consists
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