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Uva-DARE (Digital Academic Repository) UvA-DARE (Digital Academic Repository) On the Phylogeny of Halichondrid Demosponges Erpenbeck, D.J.G. Publication date 2004 Link to publication Citation for published version (APA): Erpenbeck, D. J. G. (2004). On the Phylogeny of Halichondrid Demosponges. Universiteit van Amsterdam. General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:25 Sep 2021 Chapterr 1 AA combined molecular, morphological and biochemical approach onn the phytogeny of halichondrid demosponges (Partt 1: Introduction) D.. Erpenbeck, J.A.J. Breeuwer and R.W.M. van Soest 11 1 1:: Introduction "" Indent ich mit meinen spongiologischen Untersuchungen die Saulen des Herkules iiberschreite,iiberschreite, stehe ich vor einer Aufgabe, die in ihrem ganzen Umfange nur mit den Kraften eineseines Heroen bewaltigt werden könnte. " O.E.. Schmidt 1870, Vorwort 2. Kapitel "While"While I pass with my spongiological work the columns of Hercules, I am facing a task which, to its fullfull extent, can only be performed with the strength of a hero." O.E.. Schmidt 1870, second chapter, preface Oskarr Schmidt (1870) describes in these few words the difficulties he personally experienced in workingg on the systematics of sponges, caused by the apparent simplicity of these organisms. More thann a century later these uncertainties in sponge systematics are still present at almost all taxonomie levels,, as shown in the following paragraphs of this introduction. Thiss thesis aims to contribute to a phylogeny of the demosponge order Halichondrida Gray, a groupp of demosponges that inhabits all world oceans, in almost all latitudes, from the surface down too great depths. The order is named after the genus Halichondria Fleming, and is derived from the translationn from the Greek: "cartilage of the sea" (Hansson 1994), referring to the amorphous shape andd cartilaginous consistency of many taxa. The type species of this order, the "breadcrumb-sponge" (Halichondria(Halichondria panicea Pallas 1766), belongs to the best-studied of all sponges. Despitee recent major advances in sponge systematics (Hooper and Van Soest, 2002), the phylogeneticc systematics of Halichondrida is largely unresolved notwithstanding the fact that the majorr taxa of demosponges are connected with the phylogenetic position of this order. For this reason, iss it important to discuss halichondrid systematics within the context of demosponge systematics, and vicevice versa. Thiss introduction will firstly explore to what extent systematic problems affect the highest taxonomiee level in sponges, then introduce the current demosponge orders and focus on the genera off the order Halichondrida. Finally, the pivotal role of Halichondrida will be explained in the historic contextt of sponge systematics. 1.11 Poriferan taxonomie problems: Phylum level "Thee phylum Porifera contains those animals commonly called sponges". Gribble (1998) introduces withh these words the sponges to his readers, probably bearing in mind that the taxon "Porifera" and especiallyy its metazoan (animal) entity is not commonlyy known. Over the history of their systematics (seee below), sponges have been placed in several kingdoms, but now there is no doubt they belong withinn the Metazoa. Independent of the quest for the "Urmetazoan" (Muller et al. 2001), sponges aree regarded amongst the most primitive animals and are the oldest extant animal group. First, fossil demospongee records are dated from around 750 MYA ago and their bauplan is basically unchanged sincee the Late Cambrian (509 MYA, Reitner and Wörheide 2002). The autapomorphies of the Metazoa (ass Porifera + Epitheliozoa / Eumetazoa) are (a) diploid multicellularity, (b) meiosis, (c) oogenesis (off one egg cell and three polar bodies out of one oocyte), (d) spermatogenesis (four identical sperm cellss out of one spermatocyte) and (e) the bauplan of the sperm cell itself (Ax 1995). These characters differentiatee animals clearly from their assumed closest relatives, the Choanoflagellida. Spongess are defined by their biphasic life cycle, filter feeding habit in combination with sessilee adult life form, pinacocytes, aquiferous system, choanocytes and totipotent motile cells (e.g., 12 2 1:: Introduction Axx 1995; Vacelet 1990; Hooper and Van Soest 2002). Several exceptions exist, such as sponges that lackk a mineral skeleton ("keratose" sponges and Chondrosia, Oscarella and Halisarcida), carnivorous spongess (Cladorhizidae) and (fossil and recent) choanocyte-, choanocyte-chamber-, and aquiferous- system-- lacking sponges (Thymosiopsis, Vacelet and Boury-Esnault 1995). Thee possession of (1) belt desmosomes (zonula adhaerens) to form an epithelium, (2) differentiationn of an ectoderm and entoderm and (3) digestive glands, are robust criteria to separate thee more derived animals from the sponges (Ax 1995). 1.22 Poriferan taxonomie problems: Class level Thee sponge classes are well defined: Calcarea (calcareous sponges) produce limestode "needles" (spicules)) extracellularly, Hexactinellida (glass sponges) possess a syncytium of somatic cells andd triaxonic silica spicules, and Demospongiae produce monaxonic or tetraxonic silica spicules andd secrete spongin (spongin B) via spongioblasts. Intermediate forms, called Sclerosponges (= "corallinee sponges", with a limestone basal skeleton and siliceous spicules) were initially regarded ass a fourth class of sponges, but morphological (Van Soest 1984a; Vacelet 1985) and molecular data (Chombardd et al. 1997; Cao et al. 1998; Cantino et al. 1999; Carvalho and Hajdu 2001; Casiraghi et al.. 2001) showed their polyphyletic, predominantly demosponge, origin. Conversely,, the phylogenetic relationships between the three extant sponge classes are still largelyy undecided, with several competing hypotheses: Boger (1988) divided sponges by their mineral skeletonn type and opposed Calcarea to Hexactinellida and Demospongiae ("Silicacea"). Other authors regardedd the syncytial tissue of the Hexactinellida ("Symplasma") as more discriminating and opposedd them to the non-syncytial Demospongiae and Calcarea ("Cellularia", Reiswig and Mackie 1983;; Mehl and Reitner 1996). Furthermore,, ultrastructural and molecular data provided evidence for a paraphyletic assemblagee of the three classes: Woollacott and Pinto (1995) investigated the ultrastructure of choanocytess and found the flagella bases of Calcarea closer to those of other diploblastic animals thann to Demospongiae and Hexactinellida. Thee theory of metazoan paraphyly found support in various molecular analyses, although theyy failed to provide a congruent picture. The Hsp70 data of Borchiellini et al. (1998) found sponges monophyleticc clustering at the base of the Metazoa. This was similar to the findings of Kim et al. (1999,, 18S data) and Medina et al. (2001, 18S and 28S data), which lacked sufficient support for spongee paraphyly. In Zrzavy et al.'s analysis (1998, 18S data and morphology) sponges clustered paraphyletically,, with siliceous sponges being most primitive. Adam's 18S data (1999) rejected sisterr group relationships of Calcarea to any other demosponge class. Lafay et al. (1992, 28S data) providedd the first molecular indication of a possible Calcarea - "Coelenterata" relationship, which wass subsequently supported by Cavalier-Smith et al. (1996, 18S data) and Schütze et al. (1999, HSP700 data). Collins (1998, 18S data) found Demospongiae and Hexactinellida at the base of the Metazoaa and Calcarea as (an unsupported) sister group of Ctenophora. Borchiellini et al. (2001,18S data)) and Kruse et al. (1998, cPKC data) found Calcarea as the sister group of all other diploblasts, leavingg Demospongiae and the basal Hexactinellida paraphyletic at the base of the metazoan tree. Thee caveats of sponge systematics are not restricted to the higher taxon level. The intra- ordinall relationships of the three classes are basically unresolved as well: 1.33 Poriferan taxonomie problems: Demosponge systematics Levii (1957) dubbed the Porifera as the last major group of Metazoa in which the orders were still not clearlyy defined. Difficulties are clearly due to the primitive bauplan of this taxon producing a shortage 13 3 1:: Introduction off characters required for a robust phylogenetic reconstruction. Sponges bear only a few different cell typess of which the sclerocytes produce the characteristic (if present) spicules (see glossary). These spiculess are usually arranged to form a distinct skeleton, and can be loosely distributed throughout thee sponge body without order. The size, type, shape, combination of spicules and their skeletal arrangementss are the fundaments of current sponge systematics. Although spicule morphogenesis and evolutionn
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