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(Gastropoda) with a Rhipidoglossate Radula

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(Gastropoda) with a Rhipidoglossate Radula Org Divers Evol (2011) 11:201–236 DOI 10.1007/s13127-011-0048-0 ORIGINAL ARTICLE Interactive 3D anatomy and affinities of the Hyalogyrinidae, basal Heterobranchia (Gastropoda) with a rhipidoglossate radula Gerhard Haszprunar & Erika Speimann & Andreas Hawe & Martin Heß Received: 25 January 2011 /Accepted: 26 May 2011 /Published online: 19 June 2011 # Gesellschaft für Biologische Systematik 2011 Abstract Whereas Hyalogyrina Marshall, 1988 was already on the rhipidoglossate, i.e. the ‘archaeogastropod’, originally considered a skeneid vetigastropod, the family level of evolution. Ectobranchia are considered the first Hyalogyrinidae Warén & Bouchet, 1993 has later been extant offshoot of the Heterobranchia; implications for the classified as basal Heterobranchia despite their rhipidoglossate stem species of the latter are outlined. radula. In order to evaluate this placement and to shed more light on the origin of all higher Gastropoda, we investigated Keywords Gastropoda . Ectobranchia . Hyalogyrinidae . five representatives of all three nominal hyalogyrinid genera Interactive 3D anatomy. Systematics . Phylogeny. by means of semithin serial sectioning and computer-aided Heterobranchia 3D reconstruction of the respective anatomy, which we present in an interactive way. In general the morphological features (shell, external morphology, anatomy) fully confirm Introduction the placement of Hyalogyrinidae in the Heterobranchia, but in particular the conditions of the genital system vary During the last 25 years major progress has been made in substantially within the family. The ectobranch gill of our understanding of the origin of the higher gastropods, Hyalogyrinidae is shared with Valvatidae, Cornirostridae, i.e. the allogastropod, opisthobranch and pulmonate taxa, the and Xylodisculidae; consequently all these families are latter two of which are commonly united as Euthyneura. united in Ectobranchia Fischer, 1884. The rhipidoglossate Haszprunar (1985a) first proposed the “Heterobranchia- hyalogyrinid radula suggests independent acquisition of Concept” in considering certain former ‘mesogastropods’ as taenioglossate radulae in the Caenogastropoda and other linking step by step a basal caenogastropod with a primitive Ectobranchia. Therefore, the origin of the Heterobranchia— euthyneuran level of organization. These (paraphyletic) and thus of all higher gastropods—looks to have taken place ‘allogastropods’ (called heterostrophs by some authors) include, among other taxa, Ectobranchia = Valvatoidea, Architectonicidae and Mathildidae, Omalogyridae, and Electronic supplementary material The online version of this article Rissoellidae; together with the euthyneuran groups these are (doi:10.1007/s13127-011-0048-0) contains supplementary material, classified as Heterobranchia. This concept of monophyly of which is available to authorized users. all higher Gastropoda has been elaborated further by Salvini- G. Haszprunar (*) Plawen and Haszprunar (1987) and Haszprunar (1988), and Zoologische Staatssammlung München, later confirmed by numerical cladistics of morphological Münchhausenstraße 21, characters (Ponder and Lindberg 1997)aswellasbyall 81247 Munich, Germany e-mail: [email protected] applicable molecular analyses (Aktipis et al. 2008;Colganet : : : al. 2003;DayratandTillier2003; Dinapoli and Klussmann- G. Haszprunar E. Speimann A. Hawe M. Heß Kolb 2010;Grandeetal.2008;Jörgeretal.2010; McArthur Department Biology I and GeoBio-Center, and Harasewych 2003;Wägeleetal.2008). Ludwig-Maximilians-Universität München, Großhaderner Str. 2, Based on detailed anatomical and ontogenetic studies by 82152 Planegg-Martinsried, Germany Rath (1986, 1988), Salvini-Plawen and Haszprunar (1987) 202 G. Haszprunar et al. and Haszprunar (1988) regarded the freshwater Valvatidae as (1988) mentioned above, and proposed first the formal the earliest, ‘ectobranch’ offshoot of the Heterobranchia. This inclusion of the family within the Heterobranchia. In the assumption has been supported strongly by the discovery and same year Warén et al. (1993) reported on the shell, radula, detailed conchological (heterostrophic apex, though often and live animals of the Mediterranean Xenoskenea pellucida masked by lecithotrophic mode of development), morpholog- (first described by Monterosato 1874). The heterobranch ical, and spermatological (spiral type) examinations of nature of Hyalogyrinidae was strongly supported by spermato- marine valvatid relatives, namely the Cornirostridae, logical data provided by Healy (1993)onX. pellucida and an Xylodisculidae, and Orbitestellidae by Ponder (1990a, b), unnamed “Hyalogyrina” species (possibly Xylodiscula major Healy (1990, 1993), and Warén (1992). In addition, Bandel Warén & Bouchet, 1993) from hydrothermal vents off Fiji. A (1991) described the Jurassic–Cretaceous fresh- to few years later Hasegawa (1997) described Hyalogyrina brackish-water family Provalvatidae as an extinct stem depressa from Japanese waters, and Warén et al. (1997) group of the Valvatoidea. The Devonian Palaeocarbona- named Hyalogyrina amphorae and Hyalogyra zibrowii from ria jankei, with heterostrophic shell apex and valvatoid the Mediterranean Sea. Later on, Hyalogyrina umbellifera and shell shape, might be another relative (Bandel and H. globularis were described again from hydrothermal vents Heidelberger 2002). Also recent molecular data suggest by Warén and Bouchet (2001). Sahling et al. (2002)reported Ectobranchia Fischer, 1884 (in Fischer 1880–1887) as one of another, still unnamed Hyalogyrina species living at gas the earliest extant offshoots of Heterobranchia (Dinapoli and hydrate deposits from the Cascadia convergent margin in the Klussmann-Kolb 2010;Jörgeretal.2010). North-East Pacific. Most recently Warén and Bouchet (2009) The features of the heterobranch stem species and the described Hyalogyrina rissoella from deep-sea hydrocarbon most likely sister group of Heterobranchia are still matters seeps off West Africa. of debate: Whereas Haszprunar (1988)considereda Thus, the Hyalogyrinidae presently comprise 13 extant common, monophyletic origin of Heterobranchia and species classified in three genera. Alexogyra marshalli Caenogastropoda, Ponder (1991a) and Warén et al. (1993) Bandel, 1996 from the Early Triassic St. Cassian Formation provided counter arguments in favor of an independent might be added (Bandel 1996). However, the hyalogyrinid ‘archaeogastropod’ (i.e. rhipidoglossate) origin of the anatomy has remained virtually unknown, except for the Heterobranchia. Based on their numerical cladistic analyses, data in a short summary (Speimann et al. 2007). Several Ponder and Lindberg (1997) again preferred a monophyletic preserved soft bodies of five hyalogyrinid species, which origin of Heterobranchia and Caenogastropoda, and pro- represent all three nominal genera (see below), were sent to posed a taxon Apogastropoda for the combined clade. So the first author (GH) for detailed anatomical studies (see far, the molecular data have significantly supported Acknowledgments). In order to provide a sound and monophyletic Apogastropoda (e.g. Aktipis et al. 2008; thorough data basis for further considerations and hypoth- Dinapoli and Klussmann-Kolb 2010). eses, we present here the detailed anatomical description of More than 20 years ago, Marshall (1988) described these species. Since all of them show helicoid shell and several new gastropod genera and species from biogenic soft-part morphology and quite complicated conditions, substrates at bathyal depths off New Zealand and New particularly of their genital systems, the application of South Wales. According to their trochoid-like appearance and computer-aided 3D reconstruction and interactive 3D their rhipidoglossate radula, all of these species were originally presentation is of particular advantage. classified among the Skeneidae, a lumping pot for small, trochoid-like forms. Two of Marshall’s species, Hyalogyrina glabra and Hyalogyra expansa, were exceptional: While the Material and methods protoconch is similar to those of other vetigastropods, there is more than one whorl, a condition unknown among the Material Trochoidea or Vetigastropoda in general (e.g. Bandel 1982). Nevertheless, also Hyalogyra necrophaga from the West Xenoskenea pellucida (Monterosato, 1874): The specimens African coast (Angola) was described by Rubio et al. (1992: investigated were collected in June 1988 during the fig. 3) as a skeneid vetigastropod despite a clearly visible “mission Algarve” by Serge F. Gofas in the East Atlantic hyperstrophic protoconch. off Portugal, Algarve (Chenal d’Olhao, 3–7 m, 37° 00′ N, Warén and Bouchet (1993) described Hyalogyrina 07° 51′ W), from muddy beds of Zostera. The sample has grasslei and Hyalogyra vitrinelloides from the hydrothermal been preserved very well, but the semithin sections have vent habitats of the Guaymas and Lau basins, respectively,and been largely bleached by the sealing medium used about provided SEM photographs of the shells, protoconchs, 20 years ago, cedar oil (see below). opercula, radulae, and heads. The authors erected the family Hyalogyrina glabra Marshall, 1988 is the type species of Hyalogyrinidae for these and the two species by Marshall its genus, which itself typifies the family. Material from two Interactive 3D anatomy and affinities of the Hyalogyrinidae 203 samples has been investigated: (1) Paratypes (BS 925, M. All other specimens were embedded either in Spurr’s 74981: 42° 43.9′ S, 176° 08′ E to 42° 44.0′ S, 176° 05′ E, (1969) resin or in Durcopan;
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