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Formation and Homology of Radular Teeth; a Case Study Using Columbellid Gastropods (Neogastropoda: Columbellidae)

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Formation and Homology of Radular Teeth; a Case Study Using Columbellid Gastropods (Neogastropoda: Columbellidae) /. MolL Stud. (1997), 63,65-77 © The Malacological Society of London 1997 FORMATION AND HOMOLOGY OF RADULAR TEETH; A CASE STUDY USING COLUMBELLID GASTROPODS (NEOGASTROPODA: COLUMBELLIDAE) ROBERT GURALNICK and MARTA J. de MAINTENON Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, CA Downloaded from https://academic.oup.com/mollus/article/63/1/65/978311 by guest on 23 September 2021 94720-3140 USA (Received 10 May 1996; accepted 8 August 1996) ABSTRACT mature tooth row. The evolutionary trans- formation from one radular type to another Radular morphology has contributed prominently to occurs by the gain, loss or specialization of one molluscan systematic classification, especially that of or more teeth of a particular type (Haszprunar, the Gastropoda. Inferences of homology have been based on the shape, number and position of radular 1988; Ponder & Lindberg, 19%). In this study, teeth. In this study, we demonstrate the significance we evaluate the homology of radular struc- of the mode of radular formation in assessing tures, and in particular the middle tooth, of hypotheses of homology. The columbellid radula, the columbellids using not only positional considered representative of the stenoglossate type, and morphological information but also is used as a case study. formational data. The columbellid middle tooth is acuspate, Our intent is to show that positionally spanning part of a wide membrane between two equivalent radular structures may be formed in relatively large, complex lateral teeth. We examined more than one way, using the secretion of radulae from several species with acuspate or multi- cuspate middle teeth, using histological and whole rachidian structures in columbellid gastropods mount techniques, to compare the modes of forma- as an example. The constructional process tion. Our results show that acuspate rachidian struc- determines morphology and position of the tures in the species we examined are not secreted by radular structures, and so provides a more odontoblastic fields as has been shown for radular meaningful criterion for evaluating hypotheses teeth in other taxa, but are instead produced of homology. We also discuss alternative independently by other secretory cell types. The mechanisms for the formation of radular structure can not, therefore, be considered homolo- structures using evidence from examination of gous to rachidian teeth, illustrating how different whole and sectioned columbellid radulae. formational mechanisms can produce positionally equivalent structures. We suggest not using the term Since we are focusing both on the columbellid 'rachidian' to refer to the central plate in the radula and on mechanisms by which the radula columbellid radulae. is formed, we feel it is important to provide some background information on each of these topics. INTRODUCTION The columbellid radula The radula has been considered one of the Columbellidae Swainson, 1840 is included as a most useful structures for molluscan system- family of the buccinoid neogastropods. The atics and classification. In gastropods, different columbellid radula is stenoglossate, with a radular types, congruent with anatomical char- middle plate and a single pair of lateral teeth acteristics such as the number of columellar (radular formula given as 1-1-1). Within this muscles and the number and type of ctenidia, formula the columbellid radula is distinct, and have been used to diagnose non-euthyneuran conserved in the group. Although three taxa at the ordinal level and higher (Troschel, radular structures are present, the rachidian is 1856-1893). Tooth types and formulae carry generally acuspate, and the lateral teeth are connotations of implied homology. Features of large, curved, pincer-like, and capable of these radular types include the number of rotation on bases that are narrower than those teeth and their shape and position in each of lateral teeth in other taxa. The radular 66 R. GURALNICK & MJ. de MAINTENON ribbon is long, with 80 to over 300 tooth rows membranoblastic secretion does not appear (Marcus & Marcus, 1962), and the posterior to have a profound effect on the final tooth end may protrude from the pleurembolic morphology; it primarily stiffens structures proboscis into the visceral cavity. already present (Mischor & Markel, 1984). Because many columbellid shell charac- The shape of radular components is deter- teristics are shared with other buccinoid taxa, mined by the shape, position and secretory radular morphology provides a basis for differ- rate of the apocrine cell fields that form them entiating columbellids from other buccinoids. (Mackenstadt & Markel, 1987). The radula is used extensively for classification within the family. Although the acuspate middle plate varies little and is not considered MATERIALS AND METHODS Downloaded from https://academic.oup.com/mollus/article/63/1/65/978311 by guest on 23 September 2021 to be of great systematic value, Radwin (1977) used the morphology of the lateral teeth to Representatives of four nominal columbellid taxa distinguish membership in two subfamilies, were examined to evaluate the distribution of and variation within those types has been used different modes of formation of the rachidian structure. All specimens used were adults, or nearly for generic level classification. For example, full grown. The species examined, and the sources Pseudanachis basedowi (Hedley, 1918), one of of material are: the taxa used in this study, has been included in Columbellidae based on features of lateral (1) Columbella major Sowerby, 1832: CAS 085593, tooth morphology, but it differs in other Mazatlan, Sinaloa, Mexico (two specimens) and aspects of its anatomy (de Maintenon, unpub- Bahia de las Animas, Baja California, Mexico (two lished) and its phylogenetic affinities are specimens). (2) Columbella paytensis Lesson, 1830: CAS uncertain. 096169, Paita, Peru (three specimens). (3) Euplica bidentata (Menke, 1843): specimens collected at Nancy Cove, Rottnest Island, Western Radula formation Australia (three specimens). Radular formation has been studied primarily (4) Pseudanachis basedowi (Hedley, 1918): ANSP in pulmonate gastropods (Runham, 1963; A3390, South Vietnam (three specimens); and ANSP A8874, Malaysia (two specimens). Mischor & Markel, 1984; Mackenstadt & Two methods were used in this study to provide a Markel, 1987). Mischor & Markel (1984) preliminary description of radular formation. First, demonstrated that radular formation in the generative and mature regions of whole radulae Pomacea bridgesi, a species of ampullariid, were viewed in all four species, to compare their differs significantly from radular formation in morphology during formation and maturation. pulmonates. The formational process they Second, histological sections were examined to described for Pomacea is also applicable to evaluate the cell fields associated with different Patella coendea (Peters, 1979), and is assumed stages of formation. to be true for all non-euthyneuran gastropod taxa (Mischor & Markel, 1984). /. Whole radulae In Pomacea bridgesi, the radular teeth and membrane are secreted by two different types Radulae dissected from preserved specimens were macerated for twelve hours in 25% potassium of apocrine cells, odontoblasts and mem- hydroxide (KOH). The radulae were dehydrated branoblasts (Mischor & Markel, 1984). The through an ethanol series, air dried, and mounted on membranoblasts secrete the radular membrane stubs using double-sided tape. They were examined continuously while the odontoblasts secrete using an Electroscan model E3 environmental teeth periodically. Both odontoblasts and scanning electron microscope, uncoated, at 10 kV membranoblasts are arrayed in the back of the with a chamber pressure of 3-5 Torr water vapor. radular sac, a blind pouch formed as an out- pocketing of the stomodaeum (Raven, 1958). //. Histological radular sections The radula is continually renewed post- eriorly, pushing previously formed structures We dehydrated and cleared radular sacs, probosces anteriorly toward the functional region, where or whole animals of each species, and embedded the teeth are used and worn away. After the them in paraffin. The blocks were sectioned at 7 to 10 jim using a rotary microtome. The sections were teeth and membrane are formed, muco- stained primarily in eosin/alum haematoxylin. Speci- polysaccharides and minerals are secreted onto mens were oriented to obtain either cross sections or them by supraradular and subradular epithelia sagittal sections. Sections were viewed with a light (Runham, 1963; Mischor & Mfirkel, 1984). In microscope and photographed using an attached taxa previously studied, post-odontoblastic and camera mount and Canon AE-1 camera. RADULAR HOMOLOGY 67 RESULTS caused by different timing of tooth secretion, with lateral teeth on one side forming before Whole radulae those on the other. The odontoblastic fields that secrete these structures, however, appear Micrographs of fully developed, unworn to be bilaterally symmetrical in the radular sac, radular teeth typical to each species are shown with minor variation due to cell movement in figures 1A, 2A, 3A and 4A. For direct during secretion. comparison, the posterior, generative portion Membranes in all taxa are extensive, and from the same specimens are shown in figures entirely enclose the radular ribbon such that IB, 2B, 3B and 4B. The mature regions of the the lateral membranes meet dorsally over top Downloaded from https://academic.oup.com/mollus/article/63/1/65/978311
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