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Phylogeny and Classification of Lithistid Sponges (Porifera: Demospongiae): a Preliminary Assessment Using Ribosomal DNA Sequence Comparisons

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Phylogeny and Classification of Lithistid Sponges (Porifera: Demospongiae): a Preliminary Assessment Using Ribosomal DNA Sequence Comparisons FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1994 Springer. This manuscript is an author version and may be cited as: Kelly‐Borges, M., & Pomponi, S. A. (1994). Phylogeny and classification of lithistid sponges (Porifera: Demospongiae): a preliminary assessment using ribosomal DNA sequence comparisons. Molecular Marine Biology and Biotechnology, 3(2), 87‐103. Molecular Marine Biology and Biotechnology (1994) 3(2) 87-103 Phylogeny and classification oflithistid sponges (Porifera: Demospongiae): a preliminary assessment using ribosomal DNA sequence comparisons* Michelle Kelly-Borgestt and Shirley A. Pomponi Theonella, Corallistes, Leiodermatium, and Mi­ Division of Biomedical Marine Research, Harbor crosc1eroderma, most other genera have only been Branch Oceanographic Institution, 5600 U. S. 1 rarely recorded and described from single orfrag­ North, Fort Pierce, FL 34946, U.S.A. mented specimens. Recent lithistids are found in tropical and subtropical regions, subtidally, and down to depths of 700 m (Levi, 1991). They are Abstract found on plateaus, vertical slopes, and on the Traditionally, lithistid sponges have been combined margins of continental shelves, where they can within one order linked by the common possession dominate extremely deep water sponge assem­ of an interlocking siliceous desma skeleton. How­ blages with choristid and hexactinellid sponges ever, molecular data, morphology, and paleontology (unpublished data). confirm recent hypotheses of polyphyly for this It is crucial to understand the relationship of enigmatic group of sponges. Parsimony and neigh­ genera within and between the various assemblages bor-joining analysis of partial 18S rDNA sequences of lithistids, as well as their affinities with other derived from amplified genomic rDNA of lithistids demosponge groups. Recent research has indicated and other demosponges suggest that tetracladinid that lithistids are a promising source of a multitude and dicranocladinid lithistids are monophyletic of novel chemical structures and metabolites with and closely related to choristid demosponges. antimicrobial (Matsunaga et al., 1985), antitumor Rhizomorinid families, in contrast, are indicated as (Sun and Sakemi, 1991), antifungal (Gunasekera et being polyphyletic, with a diversity of points of aI., 1991), and immunosuppressive (Longley et aI., origin within the tetractinomorph and the cerac­ 1991) activities. The lithistids are thus a group of tinomorph poriferan subclasses. These arrange­ high priority to marine natural products and drug ments are discussed in light of several hypotheses of discovery investigations. demosponge evolution. The lithistids were a dominant group of Paleo­ zoic sponges with at least 5 lineages well estab­ lished in the Ordovician (Reid, 1970), and they Introduction were among the first sponge groups to undergo Lithistids are a group of fossil and recent sponges rapid speciation. They provide nearly all of the whose skeletons are composed of articulating sili­ fossil record of the class Demospongiae (Finks, ceous desmas, which, in most species, render the 1970; Rigby, 1991), and their high fossilization sponge body solid and rock-like (Figure 1). The potential provides a substantial body of paleon­ diversity of living lithistids is relatively poor in tological evidence for assessment of modern classifi­ comparison to that of the Cretaceous fossil fauna cations and prediction of a phylogeny for the group. (Rigby, 1991); there are approximately 50 genera of Lithistids represent relict stem groups of certain living lithistids and 150 fossil genera recognized Porifera, and they are thus among a group of (Levi, 1991). With the exception of Discodermia, organisms that are a key to questions of phylogeny of the phylum Porifera. Co~tribution *Harbor Branch number 1038. Systematics 'Correspondence should be sent to this author at her present address. Although the phylogeny of the lithistid sponge is 'Present address: Department of Zoology, The Natural His­ frequently discussed (Reid, 1970; Rigby, 1991; Levi tory Museum, Cromwell Road, London SW7 5BD, UK. and Levi, 1988; Levi, 1991), many uncertainties re­ © 1994 Blackwell Scientific Publications, Inc. main in their classification, and the relationships of 87 88 M. Kelly-Borges and S.A. Pomponi Figure 1. Desmas and skeletal char­ acteristics of Lithistid sponges. (A) TetracIone desma as found in Disco­ dermia sp. (TheoneIIidae). (B) Monax­ ial dicranocIone desma as found in Corallistes fulvodesmus (CoraIIis­ tidae) (Levi and Levi, 1983). (C) A Anaxial megaclone desma as in the megamorinid Pleroma menoui (Levi and Levi, 1983). (D) SphaerocIone desma as found in Vetulina stalactites (Sollas, 1885). (E) Anaxial megaclone desma as found in Anaderma ran­ cureli (Levi and Levi, 1983). (F) In D~ most lithistids, the desmas are inter­ E locked, with adjacent spicules into a rigid articulating skeleton through zygosis of the ends of the spicules branches (zygomes). The example shown is typical of Discodermia (Theonellidae). (G) Zygosis in Coral­ listes (CoraIIistidae). (H) Arrange­ ment of the desma skeleton. Triaenes, additional microscleres, and mega­ scIeres, such as oxea, line the sponge surface or are scattered within the F G choanosome. H the group are poorly known at all systematic levels. microscleres, and the Anoplia, in which these The lithistids have traditionally been grouped spicules were absent. The Hoplophora contained 2 within a single order, Lithistida Schmidt, due to the groups, the Triaenosa and the Rhabdosa; the former common possession of desmas; however, more contained triaenes as ectosomal spicules, and the recently the group has been considered to be latter lacked triaenes. Triaenose lithistids included polyphyletic within the Demospongiae (Table 1; the families TetracIadidae (Theonella, Discodermia, see Figure 1). Although no clear indication of the Neosiphonia), Corallistidae (Corallistes, Callipel­ exact relationships have emerged, 3 groups of to), and Pleromidae (Pleroma), and the Rhabdosa triaene-bearing genera, suborders Tetracladina, Di­ contained Neopeltidae (Neopelta), ScIeritodermi­ cranocladina, and Megamorina, are thought to be dae (Scleritoderma), and Cladopeltidae (Siphon­ allied with the Choristida, and several genera idium). The suborder Anoplia contained 2 families, previously considered to be lithistid have already Azoricidae (Azorica, Tretolophus) and Anomo­ been transferred to other demosponge groups. cIadidae (Vetulina). Sollas considered that desmas Soll as (1888) derived the first comprehensive arose as a single evolutionary event; the lithistids classification of the lithistids based upon the thus formed a monophyletic group with the Chor­ presence/absence of special ectosomal spicules and istida, and the direction of descent was from the microscleres, in addition to ubiquitous desmas. The choristids towards the lithistids, in that direction order Lithistida was divided into 2 suborders, the only. Anoplid sponges, such as Vetulina, were Hoplophora, with special ectosomal spicules and regarded as the end point in a gradual simplification Molecular systematics and phylogeny of lithistid sponges 89 of the skeleton, with loss of all ectosomal spicules rized the situation by stating "in short, many and microscleres, from the triaenose lithistids uncertainties still exist in the classification of the through to the rhabdose lithistids. lithistida, and the systematics of the group is Dendy (1905), Burton (1929), and de Laubenfels relatively poorly known... we are unable to (1936) expressed the opinion that the lithistids are contribute anything new on the subject." The most polyphyletic; Burton suggested affinity of triaene­ recent paleontological systematics (Beresi and Rig­ bearing lithistids with the choristid Pachastrelli­ by, 1993; Kruse, 1991) and morphological system­ dae, Theneidae, and Stellettidae, of sigma-bearing atics treatments regard the lithistids either as lithistids with the Tetillidae (Spirophorida), of monophyletic (order Lithistida) or as incertae tylostyle-bearing lithistids with the Polymastiidae sedis within the demosponges (Figure 2). (Hadromerida), and of chela-bearing sponges with We address preliminary questions of relation­ the Myxillidae (Poecilosclerida). De Laubenfels ship between lithistid sponges and other de­ (1936) carried this classification a step further by mosponge groups utilizing the polymerase chain actually assigning various lithistid genera to fami­ reaction (PCR) technology and sequence analysis of lies within other demosponge orders, based on the 18S rONA, and we examine these relationships in apparent similarities of the accessory spicules and light of current morphology-based classifications the skeletons of those of nonlithistid demospon­ and paleontology. ges. Thus, Gastrophanella, Aciculites, and Si­ phonidium were placed in the family Gastropha­ nellidae, which was considered to be hadromerid. Results Tabropane, Amphibleptula, Desmanthus, Litho­ Two equally parsimonious trees were found using chela, and Monocrepidium were considered to be branch and bound and branch swapping algorithms of poecilosclerid affinity, specifically allied with (Figure 3). These trees differed only in the place­ sponges grouped within what was then de Lauben­ ment of Leiodermatium and Siphonidium with fels' concept of the Phorbasidae, Myxillidae, and respect to Sc1eritoderma. In the bootstrap consen­ Clathriidae,
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