195 REVIEW / SYNTHÈSE Classification and phylogeny of Hexactinellida (Porifera)1 H.M. Reiswig Abstract: Development of the present classification scheme of the class Hexactinellida was delayed because authors of the early species descriptions did not figure their specimens and few of them had access to compound microscopes necessary to visualize characters important in determining relationships. When microscopic information on spicule sym- metry became available, Wyville Thomson in 1868 recognized the distinctive triaxial symmetry of the group and named it Vitrea. Schmidt’s 1870 name, Hexactinellidae, was without the contamination associated with Thomson’s Vitrea, and gained widespread support. Through a series of proposals and refinements, the present scheme recognizes two main lineages, Amphidiscophora and Hexasterophora, differing in shape and type of their microscleres. Since these structures are generally not retained in fossil material, paleontologists have long had an independent classification for hexactinellids, but the trend to unify the systems is now nearly complete. Hypotheses on phylogeny of the group re- main virtually dependent upon scarce paleontological information, pending data from nucleic acid and protein sequence analyses that are not yet available for unravelling relationships among hexactinellids. Résumé : L’élaboration du schéma actuel de classification de la classe des Hexactinellida a été retardée parce que les descripteurs des espèces plus anciennes n’ont pas fourni d’illustrations de leurs spécimens et parce que peu d’entre eux avaient accès aux microscopes nécessaires pour voir les caractères importants dans l’établissement des relations. En 1868 au moment où ilyaeudesrenseignements sur la structure microscopique de la symétrie des spicules, Wyville Thomson a reconnu la symétrie triaxiale caractéristique du groupe qu’il a nommé Vitrea. Le nom d’Hexactinellidae proposé par Schmidt en 1870 était exempt de la contamination associée au nom Vitrea de Thomson et a été largement adopté. Après une série de propositions et de raffinements, le schéma actuel reconnaît deux lignées principales, les Amphidiscophora et les Hexasterophora, qui se distinguent par la forme et le type de leurs microsclères. Comme ces structures ne persistent généralement pas chez les fossiles, les paléontologues utilisent depuis longtemps une classifica- tion indépendante pour les hexactinelles; cependant, la tendance visant à unifier les deux systèmes est pratiquement ar- rivée à terme. Le débrouillement des relations chez les hexactinelles est basé sur des hypothèses phylogénétiques qui dépendent des rares informations paléontologiques en attendant les données non encore disponibles sur les séquences d’acides nucléiques et de protéines. [Traduit par la Rédaction] Reiswig 204 Classification: zoological versus torically and still work mainly with dredged specimens, of- paleontological ten mud-filled, with loose spicules displaced by crushing and scouring during collection, but most or all of their skele- The group of 500–600 Recent species of sponges now tal components are usually retained and can be analyzed. grouped as the class Hexactinellida originated in the Protero- Long hoped for, but rarely collected, immaculate, minimally zoic and has left a long, if not extensive, fossil record. Zool- disturbed specimens are increasingly becoming available to ogists and paleontologists working with hexactinellid these workers from submersible surveys. Paleontologists, in sponges each have access to specimens that usually differ contrast, still work with partial and extensively altered speci- strikingly in quality. Taxonomic zoologists (this author) his- mens. Soft hexactinellids with skeletons of loose (unfused) Received 15 August 2005. Accepted 21 November 2005. Published on the NRC Research Press Web site at http://cjz.nrc.ca on 3 March 2006. H.M. Reiswig.2 Natural History Section, Royal British Columbia Museum, P.O. Box 9815, Stn. Prov. Govt., Victoria, BC V8W 9W2, Canada. 1This review is one of a series dealing with aspects of the biology of the phylum Porifera. This series is one of several virtual symposia on the biology of neglected groups that will be published in the Journal from time to time. 2Present address: Department of Biology, University of Victoria, P.O. Box 3020, Stn. CSC, Victoria, BC V8W 3N5, Canada (e-mail: [email protected]). Can. J. Zool. 84: 195–204 (2006) doi:10.1139/Z05-174 © 2006 NRC Canada 196 Can. J. Zool. Vol. 84, 2006 Fig. 1. Basic outline of the present classification of scopic inspection of skeletal components. Most specimens Hexactinellida with thumbnail figures of typical body forms. have some hexactine spicules, but some have only reduced forms with one or more rays undeveloped; needle-shaped diactine spicules, where four rays have been suppressed, are sometimes the only large spicules present. Evidence of deri- vation can be found in the axial cross near the center of each spicule where remnants of reduced rays can be seen at mod- erate magnification of a compound microscope. In those fos- sil forms where only impressions of spicules remain, a level of doubt accompanies assignment of such specimens to Hexactinellida. Development of the concept: Hexactinellida The process of recognition of Recent hexactinellids as a natural group of animals required awareness of shared unique characters among a reasonable number of known specimens and species. For this group, the pre-recognition period before its erection by Schmidt in 1870 was rather ex- tended in time since deep-sea collecting was limited, micro- glass spicules are occasionally found as full body fossils, scopes were not widely available, and many of the first usually as impressions with spicule indications more-or-less specimens consisted of single fragments or incomplete spec- in place, but more commonly as only skeletal fragments of imens lacking loose spicules. The first specimen described parts of the body wall, or as individual spicules dispersed in and later recognized as a hexactinellid was the “extraordi- sediments and replaced with pyrite or other minerals. Hard nary Glass Rope” from Japan in the collections of the Brit- hexactinellids, those with skeletons of siliceous spicules ish Museum that Gray (1832) named as Hyalonema, without fused into a rigid network, are more readily preserved as species designation; he completed its binomen as H. sieboldi fossils, but even here, the complement of associated loose in 1835 (Fig. 2). He placed it among the sea pens in spicules is generally lost and details of even the fused skele- Pennatulidae and not with other sponges. A long convoluted ton can be destroyed by mineral replacement. Zoologists literature dealing with whether or not the glass rope have historically based classification of Recent Hexactinel- Hyalonema was actually part of the soft sponge located at its lida upon loose spicules, items not commonly available to base extended through the 1860s. Most correspondents ac- paleontologists. It is thus understandable that two partly in- cepted the glass rope as being part of the associated sponge, dependent classification systems have been developed for while Gray died in 1874 steadfastly refusing to accept that Recent and fossil members of this group, with various de- interpretation. grees of overlap in categories above the family level. Indeed The second hexactinellid-to-be was described, figured, many of the ordinal-level grouping now accepted in zoologi- and named Alcyoncellum speciosum by Quoy and Gaimard cal classification were developed first by paleontologists in 1833 as an amorphous zoophyte. Unfortunately the speci- (Fig. 1). Happily, there is now very strong movement by pa- men, obtained by Quoy and Gaimard on their voyage of dis- leontologists to rearrange their classification scheme to con- covery of the “Astrolabe” as a gift from the Governor of the form to that used by zoologists (Rigby 2003). Mollucas, consisted only of a rigid sac of fused siliceous fil- Classification schemes developed by both groups of work- aments (spicules) with all loose spicules washed out (Fig. 2). ers are now, and have always been, based upon details of However, the specimen had, and still has, a series of taxo- skeletal organization of these sponges. Soft tissue characters, nomic problems that remain incompletely corrected. Blain- e.g., cytological details and biochemical data such as amino ville (1830) described and named another sponge from Quoy acid and nucleotide sequences, have been available from and Gaimard’s collection, clearly what we now know as a only a few species, adequate for testing relationships be- calcareous sponge, as A. speciosum. He apparently applied tween hexactinellids and other classes of Porifera, but not Quoy and Gaimard’s manuscript name to the wrong specimen yet from a wide enough range of specimens to enable testing and attempted to rectify it soon after (Blainville 1834) by of hypotheses of relationships between groups of hexactinel- renaming the calcarean as A. gelatinosum. The genus lids formed from comparisons of the more readily preserv- homonymy was eventually corrected by Gray (1867) forming able physical elements — the shape, size, distribution, etc., the new name Corbitella for it, but the species homonymy re- of their siliceous skeletal spicules. The single diagnostic fea- mains unresolved. The third hexactinellid-to-be, eventually ture of the spicules, besides being siliceous, is that either known as “Venus’s Flower-basket” was described without fig- they