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Molecular Phylogenies Challenge the Classification of Polymastiidae (Porifera, Demospongiae) Based on Morphology

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Molecular Phylogenies Challenge the Classification of Polymastiidae (Porifera, Demospongiae) Based on Morphology Org Divers Evol (2017) 17:45–66 DOI 10.1007/s13127-016-0301-7 ORIGINAL ARTICLE Molecular phylogenies challenge the classification of Polymastiidae (Porifera, Demospongiae) based on morphology Alexander Plotkin1 & Oliver Voigt2 & Endre Willassen3 & Hans Tore Rapp1,4 Received: 13 January 2016 /Accepted: 7 August 2016 /Published online: 1 September 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Polymastiidae Gray, 1867 is a worldwide distribut- classification scheme, several strongly supported clades, ed sponge family, which has a great significance for under- which may be used as reference points in future classification, standing of the demosponge deep phylogeny since the former are recovered and three taxonomic actions are proposed: trans- order Hadromerida Topsent, 1894 has been recently split fer of one species from Radiella to Polymastia Bowerbank, based on the molecular evidence and a new separate order 1862; transfer of three species from Radiella Schmidt, 1870 to has been established for the polymastiids. However, molecular Spinularia Gray, 1867; and the consequent abandonment of data obtained from Polymastiidae so far are scarce, while the Radiella. phylogenetic reconstruction based on morphology has faced a deficit of characters along with the vagueness of their states. Keywords Phylogeny . Homoplasy . Polymastiidae . CO1 . The present study is a phylogenetic reconstruction of 28S rDNA Polymastiidae based on novel data on two molecular markers, cytochrome oxidase subunit I and large subunit ribosomal DNA, obtained from a broad set of species. Monophyly of Introduction the family and nonmonophyly of four polymastiid genera are revealed, suggesting a high level of homoplasy of mor- Polymastiidae Gray (1867), with its 122 species from 15 gen- phological characters, which are therefore not an appropriate era and a worldwide distribution (VanSoest et al. 2015), is one base for the natural classification of Polymastiidae. Although of the key families in Demospongiae Sollas, 1885, the most the presented phylogenies cannot yet provide an alternative diverse class of sponges. At the same time, Polymastiidae is one of the problematic taxa with a controversial classification (Plotkin et al. 2012). Classification of the demosponges has Electronic supplementary material The online version of this article (doi:10.1007/s13127-016-0301-7) contains supplementary material, traditionally been based on the shape and arrangement of their which is available to authorized users. skeletal elements, i.e., mineral spicules and organic fibers (Hooper and Van Soest 2002). The polymastiids possess a * Alexander Plotkin relatively simple spicule assortment providing a rather scant [email protected] set of taxonomic characters (Plotkin et al. 2012). Polymastiidae comprises sponges of various body shapes, of- 1 Department of Biology, University of Bergen, Postbox 7803, ten bearing papillae and possessing a skeleton mainly com- 5020 Bergen, Norway posed of smooth monactines (Boury-Esnault 2002; see termi- 2 Department of Earth and Environmental Sciences, Paleontology and nology of the sponge morphology in Boury-Esnault and Geobiology, Ludwig-Maximilians-Universität München, Rützler 1997). Based on the latter feature, this family was until Richard-Wagner-Str. 10, 80333, Munich, Germany recently affiliated with the demosponge order Hadromerida 3 Natural History Collections, University Museum of Bergen, Topsent, 1894. For the moment, only one morphological fea- University of Bergen, Postbox 7800, 5020 Bergen, Norway ture delimiting Polymastiidae from other demosponges is usu- 4 Centre for Geobiology, University of Bergen, Postbox 7803, ally defined, the presence of a superficial cortical palisade 5020 Bergen, Norway made of spicules differing from those composing the 46 A. Plotkin et al. choanosomal tracts in size and/or in shape (Boury-Esnault et al. 2015). In all phylogenies resulting from these studies, 2002; Plotkin and Janussen 2008). However, this feature is Polymastia was nonmonophyletic, while the family in fact also displayed by some taxa from other families, e.g., Polymastiidae was monophyletic excluding two species from by Aaptos Gray, 1867 belonging to the Suberitidae Schmidt, Nichols (2005). Furthermore, in all molecular phylogenies of 1870 (Plotkin et al. 2012). Demospongiae, Polymastiidae and other hadromerid families Discrimination between polymastiid genera is based on the appeared in remote clades that seriously contradicted the body shape (e.g., radial body in Radiella Schmidt, 1870 and traditional classification based on their morphological columnar body in Tentorium Vosmaer, 1887), the architecture similarities. Very recently, based on the molecular data, of the choanosomal skeleton (diffuse skeleton in Quasillina Morrow and Cárdenas (2015) proposed abandoning the order Norman, 1869 and Ridleia Dendy, 1888, reticulate skeleton in Hadromerida and establishing five new orders for the former Weberella Vosmaer, 1885 and radial skeleton in the remaining hadromerids, with the order Polymastiida including only one 12 genera) and the presence of spicules other than the ordinary family, the Polymastiidae. This proposal highlights the impor- smooth monactines in the choanosome (in four genera), or in tance of the polymastiids in the context of the deep phylogeny the cortex (in five genera) (Boury-Esnault 2002). However, in of demosponges. some cases, these characters are inconsistent. For example, The purpose of the present study was to reconstruct the Polymastia Bowerbank, 1862 is usually defined as sponges phylogeny of the family Polymastiidae based on two broadly with a radial choanosomal skeleton and smooth monactines used molecular markers, the 5′-end barcoding region of CO1 constituting both the choanosomal and cortical skeleton (Folmer et al. 1994) and a large region of 28S rRNA (helix (Boury-Esnault 2002) even though several species tradition- B10 to helix E19, numeration of the helices according to De ally affiliated with Polymastia display a reticulate skeleton Rijk et al. (1999, 2000)andWuytsetal.(2001)), employing a (Plotkin et al. 2012) or extraordinary spicules in the much larger set of polymastiid species than ever studied be- choanosome or in the cortex (Kelly-Borges and Bergquist fore. We also tested the monophyly of the family as well as the 1997). Other characters used in the taxonomy of polymastiids monophyly of its genera and traced the evolution of morpho- include the number of size categories of the ordinary logical characters along the branches of the consensus molec- monactines and the minute differences in their shape, the pres- ular tree. ence and architecture of additional cortical layers, and the anatomy of the papillae (Boury-Esnault 1987, 2002;Kelly- Borges and Bergquist 1997; Morrow and Boury-Esnault Material and methods 2000; Plotkin and Janussen 2008). These characters are often unstable and provide poor taxonomic information (Plotkin Sampling and taxonomic identification et al. 2012). Particularly, they fail to discriminate between some morphologically similar polymastiids, which inhabit Eighty-seven polymastiid individuals were collected for our the polar and temperate waters of the northern and southern study and deposited in the natural history collections of four hemispheres, but do not occur in the tropics, and consequent- museums (see Table 1 for details). Both the individuals in toto ly, a bipolar distribution is presumed for these species (e.g., for assigned for morphological examination and the choanosomal Tentorium semisuberites (Schmidt 1870)andRadiella sarsi pieces of about 1 cm3 for DNA extraction were fixed in 95– (Ridley & Dendy, 1886)). 100 % ethanol. Sponge anatomy was examined under a light Phylogenetic reconstruction of Polymastiidae based on 25 microscope on 500–700-μm-thick sections prepared using a binary morphological characters (Plotkin et al. 2012) precise saw with a diamond wafering blade after embedding questioned the monophyly of the family, with of tissue pieces in epoxy resin. Isolated spicules were exam- Pseudotrachya hystrix (Topsent, 1890) not grouping with ined under a light microscope and SEM. Preparations and any other polymastiid and one of the outgroup species, subsequent taxonomic identification followed well-known Aaptos papillata (Keller, 1880), joining the main polymastiid routines for polymastiids (Boury-Esnault 1987;Boury- clade, and demonstrated that Polymastia is polyphyletic. At Esnault and Bézac 2007; Plotkin and Janussen 2007, 2008). the same time, molecular phylogenies of Polymastiidae have been never properly reconstructed. Until now, common phy- Taxonomic scope logenetic markers as the barcoding regions of cytochrome oxidase subunit I (CO1) and the partial RNA from the large In our study, we included genetic data on 24 unambiguously and small ribosomal subunits (28S and 18S) have only been identified species and ten operational taxonomic units obtained for a small number of polymastiid species, aiming to (OTUs), of which four were identified to species level with resolve a deep phylogeny of the class Demospongiae instead some uncertainty and six could not be referred to any known of addressing the relationships within Polymastiidae (Nichols species and were therefore onlyidentifiedtogenuslevel 2005;Morrowetal.2012, 2013; Redmond et al. 2013; Vargas (Table 1). These species and OTUs belonged to seven Molecular phylogenies challenge classification of Polymastiidae Table 1 List of specimens
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