Development of asymmetry in the caenogastropods Amphissa columbiana and Euspira lewisii

Abstract. The asymmetry displayed by the body plan of gastropods has been directly or indirectly attributed to an evolutionary process called torsion. Torsion is defined as a rotation of 180° between the cephalopodium (head and foot) and visceropallium (visceral organs, mantle, mantle cavity, and shell). During development, the displacement of anatomical components occurs during a process called "ontogenetic torsion." Although ontogenetic torsion is central to theories of gastropod evolution, surprisingly few studies have documented actual tissue movements during the development of asymmetry in gastropods. We investigated the development of the mantle cavity and pleurovisceral nerve connective (visceral nerve loop) in the caenogastropods Amphissa columbiana and Euspira lewisii , because displacements of both of these structures are interpreted as major consequences of torsion. Scanning electron micrographs, histological sections, and immunofluorescence images showed that the developing vis-ceropallium twists by 90° relative to the cephalopodium, the mantle cavity initially forms on the right side, and displacements of the visceral nerve loop become evident on the left side before the right side. A developmental stage in which the mantle cavity is confined to the right side has also been reported in members of the Vetigastropoda and Heterobranchia. We suggest that further comparative studies should test the hypothesis that early development throughout the Gastropoda converges on an embryonic organization in which the mantle cavity and anus are located laterally, despite clade-specific differences in developmental patterns both before and after this stage.     

Early differentiating neuron in larval abalone (Haliotis kamtschatkana) reveals the relationship between ontogenetic torsion and crossing of the pleurovisceral nerve cords

Crossing of the pleurovisceral nerve cords in gastropods has supported the view that gastropods evolved by 180 degrees rotation between the ventral and dorsal body regions. Indeed, a rotation of this type occurs as a dramatic morphogenetic movement ("ontogenetic torsion") during the development of basal gastropods. According to a long-standing hypothesis, ontogenetic torsion in basal gastropods preserves an ancient developmental aberration that generated the contorted gastropod body plan. It follows from this reasoning that crossing of the pleurovisceral nerve cords during gastropod development should be mechanically coupled to ontogenetic torsion. The predicted mechanical coupling can now be examined because of the discovery of an early differentiating neuron in Haliotis kamtschatkana (Vetigastropoda) that expresses 5-hydroxytryptamine-like immunoreactivity. The neuron appeared to delineate the trajectory of the pleurovisceral nerve cords beginning before ontogenetic torsion. Before torsion, the neuronal soma is embedded in mantle epithelium at the ventral midline and two neurites extend anteriorly toward the apical sensory organ. Contrary to expectation, the two neurites of this cell did not cross-over during ontogenetic torsion because the soma of this mantle neuron shifted in the same direction as the rotating head and foot. Full crossing of the pleurovisceral nerve cords occurred gradually during later development as the mantle cavity deepened and expanded leftward. These results are consistent with a generalization emerging from comparative studies indicating a conserved developmental stage for gastropods in which the mantle cavity is localized to one side, despite a fully "post-torsional" orientation for other body components. Developmental morphology before this stage is much more variable among different gastropod clades.     

Modern insights on gastropod development: Reevaluation of the evolution of a novel body plan

More than a century of speculation about the evolutionary originof the contorted gastropod body plan has been inspired by adultanatomy and by long-standing developmental observations. Theresult has been a concept of gastropod torsion that I call the"rotation hypothesis." Under the rotation hypothesis, gastropodsoriginated when all components of the visceropallium (shell,mantle, mantle cavity with contained structures, and viscera)rotated by 180° relative to the head and foot. This evolutionaryrotation is echoed during early development of patellogastropodsand vetigastropods and occurs to some extent during developmentof more derived clades. However, comparative developmental dataon ontogenetic torsion are minimal and I argue that the rotationhypothesis is a tautological argument. More recent studies onrepresentatives from 3 major clades of gastropods suggest thatthe highly conserved aspect of gastropod development is notsynchronous rotation of all components of the visceropalliumrelative to the head and foot but rather a state of anatomicalorganization in which the developing mantle cavity is on theright but the shell coil is posterior (endogastric orientation).This conserved state of developmental anatomy has inspired analternative hypothesis for the evolutionary origin of the gastropodbody plan, the "asymmetry hypothesis." Under the asymmetry hypothesis,the gastropod mantle cavity originated from 1 side only of abilateral set of mantle cavities. The asymmetry hypothesis doesnot require a saltation event to explain the origin of gastropods,nor does it require that the ancient molluscan precursor ofgastropods carried the shell coil over the head (exogastricorientation).     

Ontogenetic Torsion and Protoconch Form in the Archaeogastropod Haliotis kamtschatkana: Evolutionary Implications

Ontogenetic torsion in archaeogastropods has strongly influenced theories about early gastropod evolution, but the seminal studies by Crofts (1937, 1955) remain the major source of information about tissue movements during this developmental process. Computer-generated reconstructions of histological sections indicate that the cephalopodium of Haliotis kamtschatkana Jonas, 1845 rotates by a full 180° relative to the shell and visceral lobe during the first quarter of pre-metamorphic development. However, a portion of pallial epithelium, including some of the shell field, accompanies the rotating cephalopodium; a process facilitated by detachment of the pallium from the apertural rim of the protoconch. Transmission electron microscopy indicates that a tract of the larval retractor muscle, which Crofts (1955) implicated in the mechanism of torsion, inserts on both pedal and pallial cells. A deep invagination of shell field epithelium is a major focus of rotational torque. As a result of pallial deformation during cephalopodial rotation, the anus and gill rudiment are restricted to the right half of the larval body for 2 days after cephalopodial rotation by 180° has been completed. Scanning and transmission electron microscopy indicate that grooves in the lateral flanks of the protoconch correspond to the deep invagination of shell field epithelium. The grooves are not created by a coiling type of accrelionary shell growth or by flexion of the protoconch. A calcareous shelf is secondarily added to the periostracal template of the protoconch along its visceral apertural rim. Morphogenetic movements during ontogenetic torsion in this species are more complex than a simple rotation between cephalopodium and visceropallium and the protoconch shows no evidence of exogastric coiling. © 1997 Published by Elsevier Science Ltd on behalf of The Royal Swedish Academy of Sciences.     

Ontogenetic torsion in two basal gastropods occurs without shell attachments for larval retractor muscles

Results of this study on two species of vetigastropods contradict the long-standing hypothesis, originally proposed by Garstang (1929), that the larval retractor muscles power the morphogenetic movement of ontogenetic torsion in all basal gastropods. In the trochid Calliostoma ligatum and the keyhole limpet Diodora aspera, the main and accessory larval retractor muscles failed to establish attachments onto the protoconch (larval shell) when the antibiotics streptomycin sulfate and penicillin G were added to cultures soon after fertilization. Defects in protoconch mineralization were also observed. Despite these abnormalities, developing larvae of these species accomplished complete or almost complete ontogenetic torsion, a process in which the head and foot rotate by 180 degrees relative to the protoconch and visceral mass. Analysis by using phalloidin-fluorophore conjugate and transmission electron microscopy showed that myofilaments differentiated within myocytes of the larval retractor muscles and adherens-like junctions formed between muscle and mantle epithelial cells in both normal and abnormal larvae. However, in abnormal larvae, apical microvilli of mantle cells that were connected to the base of the larval retractor muscles failed to associate with an extracellular matrix that normally anchors the microvilli to the mineralized protoconch. If morphogenesis among extant, basal gastropods preserves the original developmental alteration that created gastropod torsion, as proposed by Garstang (1929), then the alteration involved something other than the larval retractor muscles. Alternatively, the developmental process of torsion has evolved subsequent to its origin in at least some basal gastropod clades so that the original alteration is no longer preserved in these clades.     

Major muscle systems in the larval caenogastropod,Ilyanassa obsoleta,display different patterns of development

This study describes the anatomical and developmental aspects of muscular development from the early embryo to competent larval stage in the gastropod Ilyanassa obsoleta. Staining of F‐actin revealed differential spatial and temporal patterns of several muscles. In particular, two major muscles, the larval retractor and pedal retractor muscles originate independently and display distinct developmental patterns similar to observations in other gastropod species. Additionally, together with the larval retractor muscle, the accessory larval muscle developed in the embryo at the trochophore stage. Therefore, both these muscles develop prior to ontogenetic torsion. The pedal retractor muscle marked the most abundant growth in the mid veliger stage. Also during the middle stage, the metapodial retractor muscle and opercular retractor muscle grew concurrently with development of the foot. We show evidence that juvenile muscles, such as the buccal mass muscle and siphon muscle develop initially during the late veliger stage. Collectively, these findings substantiate that larval myogenesis involves a complex sequence of events that appear evolutionary conserved within the gastropods, and set the stage for future studies using this model species to address issues concerning the evolution and eventual fates of larval musculature in molluscs. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Sequential developmental programmes for retractor muscles of a caenogastropod: reappraisal of evolutionary homologues

Evolutionary changes in the development of shell-attached retractor muscles in gastropods are of fundamental importance to theories about the early evolution and subsequent diversification of this molluscan class. Development of the shell-attached retractor muscle (columellar muscle) in a caenogastropod has been studied at the ultrastructural level to test the hypothesis of homology with the post-torsional left retractor muscle (larval velar retractor) in vetigastropod larvae. The vetigastropod muscle has been implicated in the generation of ontogenetic torsion, a morphogenetic twist between body regions that is important to theories about early gastropod evolution. Two shell-attached retractor muscles develop sequentially in the caenogastropod, Polinices lewisii, which is a pattern that has been also identified in previous ultrastructural studies on a vetigastropod and several nudibranch gastropods. The pattern may be a basal and conserved characteristic of gastropods. I found that the first-formed retractor in larvae of P. lewisii is comparable to the larval velar retractor that exists at the time of ontogenetic torsion in the vetigastropod, Haliotis kamtschatkana. However, the post-metamorphic columellar muscle of P. lewisii is derived exclusively from part of the second-formed muscle, which is comparable to the second-formed pedal muscle system in the vetigastropod. I conclude that the post-metamorphic columellar muscle of P. lewisii, is not homologous to the larval velar retractor of the vetigastropod, H. kamtschatkana.     

Larval muscle contraction fails to produce torsion in a trochoidean gastropod.

The causes and effects of ontogenetic torsion in gastropods have been debated intensely for more than a century (1-19). Occurring rapidly and very early in development, torsion figures prominently in shaping both the larval and adult body plans. We show that mechanical explanations of the ontogenetic event that invoke contraction of larval retractor muscles are inadequate to explain the observed consequences in some gastropods. The classic mechanical explanation of Crofts (4, 5) and subsequent refinements of her explanation have been based on species with rigid larval shell properties (18, 19) that cannot be extrapolated to all gastropods. We present visual evidence of the lack of rigidity of the uncalcified larval shell in a basal trochid gastropod, Margarites pupillus (Gould), and provide photographic confirmation of our prediction that larval retractor muscle contraction is insufficient to produce more than local deformation or dimpling at the site of muscle insertion. These findings do not refute muscular contraction as a primary cause of ontogenetic torsion in gastropods that calcify their larval shells prior to the onset of torsion, nor do they refute the monophyly of torsion. They do, however, suggest that torsion may be a loosely constrained developmental process with multiple pathways to the more constrained end result (20, 21).     

Turning snails into slugs: induced body plan changes and formation of an internal shell

The archetypal body plan of conchiferan molluscs is characterized by an external calcareous shell, though internalization of shells has evolved independently in a number of molluscan clades, including gastropod families. In gastropods, the developmental process of torsion is regarded as a hallmark that is associated with a new anatomical configuration. This configuration is present in extant prosobranch gastropod species, which predominantly bear external shells. Here, we show that short-term exposure to platinum during development uncouples at least two of the processes associated with torsion of the freshwater snail Marisa cornuarietis. That is, the anus of the treated snails is located anteriorly, but the gill and the designated mantle tissue remains in a posterior location, thus preventing the formation of an external shell. In contrast to the prosobranchian archetype, platinum treatment results in the formation of a posterior gill and a cone-shaped internal shell, which persists across the lifetime. This first finding of artificially induced snail-slug conversion was also seen in the pulmonate snail Planorbarius corneus and demonstrates that selective alteration of embryonic key processes can result in fundamental changes of an existing body plan and-if altered regulation is inherited-may give rise to a new one.     

Developmental modularity and phenotypic novelty within a biphasic life cycle: morphogenesis of a cone snail venom gland

The venom gland of predatory cone snails (Conus spp.), which secretes neurotoxic peptides that rapidly immobilize prey, is a proposed key innovation for facilitating the extraordinary feeding behaviour of these gastropod molluscs. Nevertheless, the unusual morphology of this gland has generated controversy about its evolutionary origin and possible homologues in other gastropods. I cultured feeding larvae of Conus lividus and cut serial histological sections through the developing foregut during larval and metamorphic stages to examine the development of the venom gland. Results support the hypothesis of homology between the venom gland and the mid-oesophageal gland of other gastropods. They also suggest that the mid-region of the gastropod foregut, like the anterior region, is divisible into dorsal and ventral developmental modules that have different morphological, functional and ontogenetic fates. In larvae of C. lividus, the ventral module of the middle foregut transformed into the anatomically novel venom gland of the post-metamorphic stage by rapidly pinching-off from the main dorsal channel of the mid-oesophagus, an epithelial remodelling process that may be similar to other cases where epithelial tubes and vesicles arise from a pre-existing epithelial sheet. The developmental remodelling mechanism could have facilitated an abrupt evolutionary transition to the derived morphology of this important gastropod feeding innovation.     

Beiträge zur Torsion und Frühevolution der Gastropoden

Contributions to torsion and early evolution of the gastropods The phylogenetical model, which is presented here, is directed by trying to explain torsion of gastropods out of biomechanical conditions. It is based on morphological and functional reflexions upon the evolution of an ancestral mollusc out of an annelid-like segmented coelomate and further evolution of this to a monoplacophoran. Starting point of gastropod evolution is a high-arched monoplacophoran with serial pairs of dorsoventral muscles. There are always alternating one pair of vertically and one pair of obliquely running, crossed dorsoventral muscles. Evolution of higher arches causes a reduction of many dorsoventral muscles and a magnification of the pallial cavity. This gives place for a few pairs of massive gills instead of many serrated little monoplacophoran gills. A second consequence is a waist (“Taille”) between cephalopodium and visceral hump. It functions as an axis for at first little, with further muscle reductions greater torsional motions of the shell and the visceral hump. At last there exists only one pair of oblique and crossed dorsoventral muscles. This situation forces a fixation of the torted position, because it causes less energy consumption. There is also a lot of other advantages for the “torted gastropod”. The construction of a bilateral ancestor is the base for the evolution of recent asymmetric snails as a bundle of different phylogenetic lines.     

Metamorphic remodeling of a planktotrophic larva to produce the predatory feeding system of a cone snail (Mollusca, Neogastropoda)

I used histological sections and 3D reconstructions to document development through metamorphosis of the foregut and proboscis in the conoidean neogastropod Conus lividus. A goal was to determine how highly derived features of the post-metamorphic feeding system of this gastropod predator develop without interfering with larval structures for microherbivory. A second goal was to compare foregut development in this conoidean with previous observations on foregut development in the buccinoidean neogastropod Nassarius mendicus. These two neogastropods both have a feeding larval stage, but they show major differences in post-metamorphic foregut morphology. Basic events in development of the proboscis and proboscis sheath in C. lividus and N. mendicus were similar. However, the elongate buccal tube of C. lividus forms during metamorphosis as a composite of apical epidermal tissue that grows inward and ventral foregut tissue that extends outward. The larval mouth is not carried through metamorphosis. Comparative observations on foregut development in caenogastropods, which now include data on C. lividus, suggest that the foregut incorporates dorsal and ventral modules having different ontogenetic and functional fates. This developmental modularity may have facilitated evolutionary diversification of the post-metamorphic foregut. Foregut diversification in predatory gastropods may have been further fast-tracked by developmental uncoupling of larval and post-metamorphic mouths.     

Torsion in Patella caerulea (Mollusca, Patellogastropoda): ontogenetic process, timing, and mechanisms

Abstract. Torsion is a process in gastropod ontogenesis where the visceral body portion rotates 180° relative to the head/foot region. We investigated this process in the limpet Patella caerulea by using light microscopy of living larvae, as well as scanning electron microscopy (SEM) of larvae fixed during the torsion process. The completion of the 180° twist takes considerably less time in larvae of Patella caerulea than previously described for other basal gastropod species. At a rearing temperature of 20–22°C, individuals complete ontogenetic torsion in ?2 h. Furthermore, the whole process is monophasic, i.e., carried out at a constant speed, without any evidence of distinct ‘fast” or ‘slow” phases. Both larval shell muscles—the main and the accessory larval retractor—are already fully contractile before the onset of torsion. During the torsion process both retractors perform cramp‐like contractions at ～30 s intervals, which are followed by hydraulic movements of the foot. However, retraction into the embryonic shell occurs only after torsion is completed. The formation of the larval operculum is entirely in‐dependent from ontogenetic torsion and starts before the onset of rotation, as does the mineralization of the embryonic shell. The reported variability regarding the timing (mono‐ versus biphasic; duration) of torsion in basal gastropod species precludes any attempt to interpret these data phylogenetically. The present findings indicate that the torsion process in Patella caerulea, and probably generally in basal gastropods, is primarily caused by contraction of the larval shell muscles in combination with hydraulic activities. In contrast, the adult shell musculature, which is independently formed after torsion is completed, does not contribute to ontogenetic torsion in any way. Thus, fossil data relying on muscle scars of adult shell muscles alone appear inappropriate to prove torted or untorted conditions in early Paleozoic univalved molluses. Therefore, we argue that paleontological studies dealing with gastropod phylogeny require data other than those based on fossilized attachment sites of adult shell muscles.     

Myogenesis in Aplysia californica (Cooper, 1863) (Mollusca,Gastropoda, Opisthobranchia) with special focus on muscular remodeling during metamorphosis

To date only few comparative approaches tried to reconstruct the ontogeny of the musculature in invertebrates. This may be due to the difficulties involved in reconstructing three dimensionally arranged muscle systems by means of classical histological techniques combined with light or transmission electron microscopy. Within the scope of the present study we investigated the myogenesis of premetamorphic, metamorphic, and juvenile developmental stages of the anaspidean opisthobranch Aplysia californica using fluorescence F‐actin‐labeling in conjunction with modern confocal laser scanning microscopy. We categorized muscles with respect to their differentiation and degeneration and found three true larval muscles that differentiate during the embryonic and veliger phase and degenerate during or slightly after metamorphosis. These are the larval retractor, the accessory larval retractor, and the metapodial retractor muscle. While the pedal retractor muscle, some transversal mantle fibers and major portions of the cephalopedal musculature are continued and elaborated during juvenile and adult life, the buccal musculature and the anterior retractor muscle constitute juvenile/adult muscles which differentiate during or after metamorphosis. The metapodial retractor muscle has never been reported for any other gastropod taxon. Our findings indicate that the late veliger larva of A. californica shares some common traits with veligers of other gastropods, such as a larval retractor muscle. However, the postmetamorphic stages exhibit only few congruencies with other gastropod taxa investigated to date, which is probably due to common larval but different adult life styles within gastropods. Accordingly, this study provides further evidence for morphological plasticity in gastropod myogenesis and stresses the importance of ontogenetic approaches to understand adult conditions and life history patterns. J. Morphol., 2008. © 2007 Wiley‐Liss, Inc.     

GASTROPOD CHEMORECEPTION

(I). Gastropods use chemoreception for a wide variety of behaviours including feeding, homing, escape from predators and a variety of social and reproductive behaviours. Chemoreception is used to locate distant food sources, and to discriminate between potential foods. Responses to chemical food stimuli result from a combination of innate and experiential factors. Gastropods use chemical cues in mucus trails to home. They also home by direct olfactory orientation. Reproductive behaviour in a variety of gastropods appears to involve chemical cues. Evidence exists for pheromones controlling aggregation and mating. Numerous gastropods use chemical cues to avoid or escape from predators. (2). Amino acids appear as likely candidates for attractants and phagostimulants for gastropod feeding. Macromolecules are probably also involved. Amino acids have also been shown to stimulate reproductive behaviours in certain gastropods, thus suggesting a pheromonal function. However, the significance of this finding to the behaviour of the organisms in the field has yet to be evaluated. Saponins have been implicated as the active substances found in sea stars that elicit escape responses of marine gastropods. Choline esters may play a homologous role in gastropod—prey and gastropod-predator interactions. (3). Gastropods can apparently use a number of different methods to orient to olfactory cues. These include anemotaxis or rheotaxis, klinotaxis and tropotaxis. (4). The major chemosensory organs of gastropods have been identified. They include the anterior and posterior tentacles and lips of terrestrial pulmonates; the cephalic tentacles, the lips and buccal cavity lining, and possibly the osphradium of aquatic pulmonates; the cephalic and mantle tentacles, the anterior margin of the foot, the siphon tip, and the osphradium of prosobranchs; and the rhinophores, tentacles, oral veil and osphradium of opisthobranchs. (5). Many of the organs named above have been examined by both light and electron microscopy. The most common anatomical organization includes bipolar primary sensory cells with cell bodies located subepithelially, and a distal dendrite extending to the free surface. Often a peripheral ganglion is located deep to the sensory epithelium. It is unclear whether axons of the sensory cells project directly to the central ganglion or by way of interneurones located in the peripheral ganglia. (6). The dendritic specializations of the sensory cells vary considerably. Most bear cilia or a combination of cilia and microvilli. The functional significance of the variation in the types of sensory endings is unknown, although the chemosensory epithelia also respond to other sensory modalities, and it is often difficult to ascribe any one cell type to any one modality. Species-specific variations may also complicate the picture. (7). Prospects for and importance of future studies on gastropod chemoreception are discussed.     

Endoscopy of gastropods: A novel view of the mantle cavities and gills of the keyhole limpet Diodora aspera and the abalone Haliotis rufescens

The gills, or ctenidia, of marine gastropods serve as the sites for respiratory gas exchange. Cilia on the surface provide the pump that moves water through the mantle cavity and enhance diffusion. Because the gills are housed inside the shell, it is difficult to view them while they are functioning. Published images of gills show contracted, fragile structures that are distorted by the processes of dissection and preservation. Members of the families Fissurellidae (keyhole limpets) and Haliotidae (abalone) have openings in their shells through which water enters and/or exits. I inserted an endoscope connected to a video camera into the openings of the shells of living, non‐anaesthetized individuals of the fissurellid Diodora aspera and the haliotid Haliotis rufescens. In both species, the dorsal afferent branchial vessel of the afferent gill axis appeared large and inflated, as did the leaflets that extended from either side of the axis. In D. aspera, the leaflets appeared to fill the mantle cavity and responded to touch, particles, and dye in the water by contracting quickly and slowly re‐extending. In contrast, the gills of H. rufescens did not noticeably respond to disturbance. On the other hand, these gills showed a regular pattern of pleats that had not been described in the extensive anatomical literature of these common and economically significant animals. These results provide a novel view of the gastropod mantle cavity as a dynamic space filled by the gills, which divide the mantle cavity into distinct incurrent and excurrent chambers and produce a laminar flow of water through the cavity. J. Morphol. 276:787–796, 2015. © 2015 Wiley Periodicals, Inc.     

Rhogocytes in gastropod larvae: developmental transformation from protonephridial terminal cells

Rhogocytes, terminal cells of protonephridia, and podocytes of metanephridial systems share an architectural feature that creates an apparent sieving device. The sieve serves to ultrafilter body fluid during the excretion and osmoregulation process carried out by nephridial systems, but its function in rhogocytes is unclear. Rhogocytes are molluscan hemocoelic cells that appear to have various functions related to metabolism of metal ions, including synthesis of hemocyanin in some gastropods and metal detoxification in pteriomorph bivalves. A hypothesis that proposed developmental and possibly evolutionary conversion between protonephridial terminal cells and rhogocytes has never been further explored; indeed, information on the occurrence of rhogocytes in molluscan developmental stages is meager. We used transmission electron microscopy to show that rhogocytes are present within larvae of eight species of gastropods sampled from the three major gastropod clades with a feeding larval stage in the life history. In larvae of a heterobranch gastropod, a rhogocyte was located next to each terminal cell of a pair of protonephridia that flanked the foregut, whereas all six species of caenogastropod larvae and a neritimorph larva that we examined had rhogocytes, but no protonephridia, in this location. We did not find ring‐shaped profiles of hemocyanin decamers within rhogocytes of larvae or pre‐hatch embryos. Rhogocytes in newly released larvae of Nerita melanotragus contained orderly bundles of cylinders, but the diameter of the cylinders was only 70% of the diameter typical of hemocyanin multidecamers. By examining embryos of the caenogastropod Nassarius mendicus at four successive developmental time points that bracketed the occurrence of larval hatching, we found that terminal cells from non‐functional protonephridia in pre‐hatch embryos transformed into rhogocytes around the time of hatching. This empirical evidence of ontogenetic transformation of protonephridial terminal cells into rhogocytes might be interpreted as developmental recapitulation of an evolutionary transition that occurred early in molluscan history.     

Pelagiella exigua,an early Cambrian stem gastropod with chaetae: lophotrochozoan heritage and conchiferan novelty

Exceptionally well-preserved impressions of two bundles of bristles protrude from the apertures of small, spiral shells of Pelagiella exigua, recovered from the Kinzers Formation (Cambrian, Stage 4, ‘Olenellus Zone’, c. 512 Ma) of Pennsylvania. These impressions are inferred to represent clusters of chitinous chaetae, comparable to those borne by annelid parapodia and some larval brachiopods. They provide an affirmative test in the early metazoan fossil record of the inference, from phylogenetic analyses of living taxa, that chitinous chaetae are a shared early attribute of the Lophotrochozoa. Shells of Pelagiella exhibit logarithmic spiral growth, microstructural fabrics, distinctive external sculptures and muscle scars characteristic of molluscs. Hence, Pelagiella has been regarded as a stem mollusc, a helcionelloid expressing partial torsion, an untorted paragastropod, or a fully torted basal member of the gastropod crown group. The inference that its chaeta-bearing appendages were anterior–lateral, based on their probable functions, prompts a new reconstruction of the anatomy of Pelagiella, with a mainly anterior mantle cavity. Under this hypothesis, two lateral–dorsal grooves, uniquely preserved in Pelagiella atlantoides, are interpreted as sites of attachment for a long left ctenidium and a short one, anteriorly on the right. The orientation of Pelagiella and the asymmetry of its gills, comparable to features of several living vetigastropods, nominate it as the earliest fossil mollusc known to exhibit evidence of the developmental torsion characteristic of gastropods. This key adaptation facilitated an evolutionary radiation, slow at first and rapid during the Ordovician, that gave rise to the remarkable diversification of the Gastropoda.