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Molecular and Morphological Data from Thoosidae in Favour of the Creation of a New Suborder of Tetractinellida

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Molecular and Morphological Data from Thoosidae in Favour of the Creation of a New Suborder of Tetractinellida Systematics and Biodiversity ISSN: 1477-2000 (Print) 1478-0933 (Online) Journal homepage: https://www.tandfonline.com/loi/tsab20 Molecular and morphological data from Thoosidae in favour of the creation of a new suborder of Tetractinellida JosÉ Luis Carballo, Eric Bautista-Guerrero, Paco CÁrdenas, Jose Antonio Cruz- Barraza & Jose Maria Aguilar-Camacho To cite this article: JosÉ Luis Carballo, Eric Bautista-Guerrero, Paco CÁrdenas, Jose Antonio Cruz-Barraza & Jose Maria Aguilar-Camacho (2018) Molecular and morphological data from Thoosidae in favour of the creation of a new suborder of Tetractinellida, Systematics and Biodiversity, 16:5, 512-521, DOI: 10.1080/14772000.2018.1457100 To link to this article: https://doi.org/10.1080/14772000.2018.1457100 Published online: 11 May 2018. Submit your article to this journal Article views: 224 View related articles View Crossmark data Citing articles: 3 View citing articles Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tsab20 Systematics and Biodiversity (2018), 16(5): 512–521 Research Article Molecular and morphological data from Thoosidae in favour of the creation of a new suborder of Tetractinellida JOSE LUIS CARBALLO1, ERIC BAUTISTA-GUERRERO2, PACO CARDENAS 3, JOSE ANTONIO CRUZ-BARRAZA1 & JOSE MARIA AGUILAR-CAMACHO4 1Instituto de Ciencias del Mar y Limnologıa, Universidad Nacional Autonoma de Mexico (Unidad Academica Mazatlan), Avenida Joel Montes Camarena s/n, Mazatlan (SIN) 82000, PO Box 811, Mexico 2Laboratorio de Ecologıa Marina, Centro de Investigaciones Costeras, Centro Universitario de la Costa, Universidad de Guadalajara, Av. Universidad No. 2013 Del, Ixtapa, Puerto Vallarta, Jalisco, CP 48280, Mexico 3Division of Pharmacognosy, Department of Medicinal Chemistry, BioMedical Center, Husargatan 3, Uppsala University, Uppsala, 751 23, Sweden 4Zoology, Ryan Institute, School of Natural, Sciences, National University of Ireland Galway, University Road, Galway, Ireland (Received 20 July 2017; accepted 7 March 2018) The Thoosidae (Porifera, Demospongiae, Tetractinellida) currently includes the genera Thoosa, Alectona, and Delectona. To this date, molecular data are only available for Alectona. In this study, the phylogenetic affinities of the genera Thoosa and Alectona have been investigated with the species T. mismalolli, T. calpulli, and T. purpurea from the Mexican Pacific using morphology and three molecular loci: the mitochondrial cytochrome oxidase subunit 1 (CO1 mtDNA), 28S rRNA (fragment D2), and 18S rRNA. Morphology and embryology showed that these genera are quite different from the rest of the tetractinellids because larvae of Alectona and Thoosa have unique features in sponges, such as the presence of monaxonic discs in Thoosa and tetraxonic discs in Alectona which disappear in the adult stages. A phylogenetic analysis using selected species from the order Tetractinellida revealed that Thoosa groups with Alectona thus confirming morphological studies. The peculiarities in spiculation and embryology of the Thoosa and Alectona larvae, which are markedly different from species belonging to the suborders Astrophorina and Spirophorina and their distant phylogenetic position (based on three molecular loci), suggest that Thoosidae could be placed in the new suborder Thoosina. Key words: Astrophorina, molecular markers, Porifera, systematics, synapomorphy, Thoosidae Introduction megascleres and triaenes in various shapes; microscleres include sigmaspires, asters, microrhabds, microxeas, or The combination of molecular phylogeny with the tradi- raphides (Morrow & Cardenas, 2015). tional morphological characters in sponge systematics The monophyly of Tetractinellida is clearly supported has showed incongruence in some orders and families by morphological and molecular data (Borchiellini, (Morrow & Cardenas, 2015; Morrow et al., 2013; Alivon, & Vacelet, 2004; Chombard, Boury-Esnault, & Redmond et al., 2011), which has led to major changes in Tillier, 1998; Erpenbeck et al., 2007; Kelly & Cardenas, the higher classification of the Demospongiae; the class 2016; Lavrov, Wang, & Kelly, 2008; Nichols, 2005). with the greatest number of species (Van Soest et al., However, the first comprehensive molecular phylogenetic 2012). The current classification divides Demospongiae study of the suborder Astrophorina showed that some into three subclasses: Verongimorpha, Keratosa, and families and genera are polyphyletic (Cardenas, Xavier, Heteroscleromorpha with 22 orders, some of them Reveillaud, Schander, & Rapp, 2011). One of those poly- recently created, or resurrected, such as the order Tetracti- phyletic families is Alectonidae Rosell, 1996 with a par- nellida, divided into two suborders: Astrophorina and ticularly unstable taxonomic history due to its boring Spirophorina. The species of this order possess monactine habitus, spicule morphology, and larval features. Alectona was first classified in the family Clionaidae dOrbigny, Correspondence to: J. L. Carballo. E-mail: [email protected]. 1851 (order Hadromerida) (Rutzler€ & Stone, 1986), and unam.mx ISSN 1477-2000 print / 1478-0933 online Ó The Trustees of the Natural History Museum, London 2018. All Rights Reserved. http://dx.doi.org/10.1080/14772000.2018.1457100 Published online 11 May 2018 A new suborder of Tetractinellida 513 later it was moved to the new family Alectonidae with the interesting character shared by Thoosa and Alectona is genera Thoosa Hancock, 1849 and Delectona de the pit pattern made during the process of bioerosion, Laubenfels, 1936, as a part of the order Hadromerida different to those produced by other boring sponges (Rosell, 1996). (Borchiellini et al., 2004; Calcinai, Bavestrello, & Cer- Vacelet (1999) suggested moving Alectona Carter, rano, 2004). 1879 to Astrophorida because of the morphology of the However, despite the morphological, cytological, and spicules in the larvae (tetraxonic discs and amphiasters) especially embryological evidence that suggest the group- which are similar to some astrophorid species. Neverthe- ing of Alectona with Thoosa, and their uniqueness less, Rutzler€ (2002a) included this genus with other boring amongst the Tetractinellida, we are still missing molecu- sponges such as Dotona Carter, 1880, Spiroxya Topsent, lar data from Thoosa species to support this recommenda- 1896, Neamphius de Laubenfels, 1953, Scolopes Sollas, tion. In the Mexican Pacific, three Thoosa species have 1888 and Delectona de Laubenfels, 1936, in the family been described (Carballo, Cruz-Barraza, & Gomez, 2004; Alectonidae while Thoosa remained in the family Clionai- Cruz-Barraza, Carballo, Bautista-Guerrero, & Nava, dae (Rutzler,€ 2002b). 2011), and the reproductive cycle is known for one of Borchiellini et al. (2004) by using a fragment of the 28S them (Bautista-Guerrero, Carballo, & Maldonado, 2010). rRNA confirmed that Alectona millari Carter, 1879 (type The aim of this work was to assess the systematic position species of the genus) was more closely related to astro- of species belonging to the genus Thoosa using three inde- phorids than to hadromerids. Cardenas et al. (2011) pendent loci: CO1 mtDNA, 28S rRNA (D2), and 18S reached the same conclusion by using the CO1 mtDNA; rRNA. Our results confirm that Thoosa and Alectona are although the sequence of A. millari did not cluster within closely related in the family Thoosidae. On the basis of any of the astrophorid clades. Interestingly, the sequence morphological and molecular differences with suborders diverged between the major clades of Astrophorina and Astrophorina and Spirophorina, we propose the creation Spirophorina which seems to suggest a pivotal evolution- of the new suborder Thoosina. ary step between the two suborders. However, the sequence of Neamphius huxleyi (Sollas, 1888), (with amphiasters but no triaenes), grouped more closely to Materials and methods desma-bearing astrophorids (Cardenas et al., 2011). Thus, Specimens of Thoosa mismalolli Carballo, Cruz-Barraza the family Thoosidae Cockerell, 1925 was resurrected &Gomez, 2004 and T. calpulli Carballo, Cruz-Barraza & (non Alectonidae because Thoosa was described before Gomez, 2004 were collected by scuba diving in a shallow Alectona) to include Thoosa, Alectona, Delectona but not (5–9 m depth) coral community surrounding Isabel Island, Neamphius de Laubenfels, 1953, considered as incertae Mexico (2152 03000N, 10554 05400W). Specimens of sedis (Cardenas & Rapp, 2012). T. purpurea Cruz-Barraza, Carballo, Bautista-Guerrero & In summary, different authors suggested the reallo- Nava, 2011 were collected from Islas Revillagigedo cation of Thoosa and Delectona along with Alectona (1934 05700N, 11103 05700W) also by scuba diving at in Thoosidae, because they share important morpholog- 5–7 m depth. Specimens were deposited in ’Coleccion de ical and biological features. They are excavating, and Esponjas del Pacıfico’ (LEB-ICML-UNAM) (Table 1). at least Thoosa and Alectona produce an unusual hopli- tomella larva, which has particular spicules that are Alectona sp. 1 was collected in the Flemish Cap, off New- different from those observed in adult stages (Bautista- foundland (4800.0031 0N, 4445.0644 0W) at a depth of Guerrero, Carballo, Aguilar-Camacho, & Sifuentes- 1554 m (NEREIDA 0509 campaign, field# DR10-056) Romero, 2016;Topsent,1920; Vacelet, 1999). Another (GeneBank accession COI MH256567; 18S MH256569). Table 1. Localities of sponge specimens, museum voucher numbers, GB and ENA accession numbers used in this study.
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