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1 Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, California 94720
2 Kewalo Marine Laboratory, University of Hawaii, 41 Ahui Street, Honolulu, Hawaii 96813, and Department of Zoology, University of Hawaii at Manoa, Honolulu, Hawaii 96822
* To whom correspondence should be addressed. E-mail: caroleh{at}socrates.berkeley.edu.
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).
Torsion is defined as an ontogenetic process that twists the gastropod larval head and foot counterclockwise by 180° relative to the underlying (in the swimming larva) shell with its mantle epithelium and visceral mass. The process is recognized morphologically by its developmental consequence: a new anatomical configuration in which the mantle cavity, anus, and gill rudiment are positioned over the head. Torsion has been regarded as the hallmark of the Gastropoda (8), the evolutionary novelty or shared derived character defining this class of molluscs. When treated as a homologous feature throughout Gastropoda, torsion tends to take on a structural definition synonymous with the torted anatomical condition.
As an ontogenetic event, torsion occurs early in larval development and may be completed in as little as 2 min (22). Crofts’ explanation (4,5) of the mechanism initiating developmental rotation in the trochid gastropod Calliostoma zizyphinum, the abalone Haliotis tuberculata, and the patellid limpet Patella vulgata involved contraction of a larval retractor muscle and assumed that the larval shell on which the muscle is inserted is calcified or at least rigid. Crofts (5) constructed wax models of gastropod larvae that were designed to illustrate the rotation by pulling on a string that was attached to the foot and threaded through a hole in the shell at the point of insertion of the larval retractor muscle. The use of working models of torsion appears to have been widespread in Britain. Eales (7) referred to a working model constructed much earlier by Ray Lancaster, and she borrowed Crofts’ models and made a set that she used in her presidential address to the Malacological Society of London (7). Physical models used "to illustrate the torsion process" (5) did not accurately simulate muscle contraction; but because they replicated the observed twist, they supported the theory of muscle contraction over differential growth as an explanation of torsion.
Although the onset of torsion and its completion are readily observed in populations of developing larvae of many species (pers. obs.), the underlying mechanism and details of the morphogenetic movements cannot be resolved (18). Debates over both the morphological changes and the underlying mechanisms have been based more on conjecture than on actual observation. Bandel (23) hypothesized that torsion in trochoidean gastropods was solely a consequence of differential growth, in contrast to the mechanism Wanninger et al. (19) described in patelloidean gastropods, which involved an alternation of muscle contractions and hydraulic swelling of the larval foot. Page (18), in a careful study of sectioned larvae of the haliotid gastropod Haliotis kamtschatkana Jonas, presented evidence that is consistent with potential roles for both muscle contraction and differential growth. In both Haliotis and Patella the larval shell is calcified at the onset of torsion (18,19).
Can larval muscle contraction provide a global explanation of ontogenetic torsion? Our observations of early larval development in trochoidean gastropods led us to hypothesize that the thin organic larval shell was insufficiently calcified at the onset of torsion and lacked the mechanical rigidity to antagonize contraction of the larval retractor muscles. Contraction of a muscle inserted on a thin organic shell should produce, instead, only a local deformation.
During the late spring and early summer of 1994, representatives of the major clades of primitive marine gastropods (informally known as archaeogastropods) were spawned at the Friday Harbor Laboratories for comparative observations of larval development and changes in shell secretion at metamorphosis. Larvae of the margaritine trochid Margarites pupillus Dall were videotaped as trochophores and pre- and post-torsional veligers; further observations were made using a combination of standard brightfield light microscopy, polarizing microscopy, and differential interference contrast microscopy.
Larvae developed rapidly (at 12°C) to the pre-torsional veliger stage within the egg envelope prior to hatching, and had secreted a cap-shaped, transparent organic shell by 48 h post-fertilization (Fig. 1a). Although the initial shell was weakly birefringent, it collapsed and crumpled at this stage (between 48 and 72 h) when attempts were made to make preparations for scanning electron microscopy. We inferred that the primordial shell was not rigid at this stage, even if weakly calcified.
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Only by videotaping larvae and examining individual frames was it possible to identify sites of apparent muscle attachment (Fig. 1b). The central observation of this paper is that the normally rounded larval shells (Fig. 1a, b) show a periodic transitory dimpling at the site of attachment of a larval retractor muscle (Fig. 1b, c). We argue that the dimpling refutes a mechanical explanation of torsion in this species. Because the dimpling is not permanent, because the active larva is constantly and rapidly changing its orientation, and because the entire shell cannot be kept in focus, the dimple is visible only periodically and for a fraction of a second at a time.
We originally intended to address the further question of whether larval muscle contraction could explain the putative mechanical deformation of the larval shell first proposed by Bandel (24). Subsequently formalized by Morita (25) as "Bandel’s Rule," the idea of mechanical deformation has been linked both with torsion and with the initiation of shell coiling. It is based on the observation that the larval shells of many "archaeogastropods" have protuberant lobes bordered by lateral grooves, giving the shell a coiled appearance. Our observations of transitory dimpling of the larval shell in response to muscle contraction suggest that much more powerful forces are required to permanently deform the symmetrical larval shell as a means of giving rise to the initial coil. At least in Margarites pupillus, shell morphogenesis is not explained by Bandel’s Rule.
Two other studies now provide a more direct critique of Bandel’s Rule (18,26). Collin and Voltzow (26) have shown that mechanical deformation cannot explain the initiation of shell coiling in the abalone Haliotis kamtschatkana, because the larval shell is fully calcified and rigid when the alleged deformation occurs. Page (18) provides an elegant alternative explanation of the underlying observations through detailed histological investigation of development in H. kamtschatkana. The creases in the lateral flank of the protoconch correspond precisely with deep visceral clefts (indentations of the shell field epithelium) in the developing larva. Her observations show that the topography of the larval shell is superimposed on the indented topography of the visceral lobe of the larva.
Our observations of transitory dimpling at the site of muscle insertion on the flexible larval shell in a phylogenetically basal trochid gastropod clade (27) immediately prior to torsion show that muscle contraction is inadequate to explain the 180° rotation of the larval head and foot (cephalopodium) relative to the shell, primordial mantle complex, and visceral mass (visceropallium). However, extrapolation of these results to all gastropods is unwarranted. In patellid and haliotid gastropods the shell is calcified and rigid at the onset of torsion and may facilitate the process in an immediate mechanical sense (18,19). In Calliostoma ligatum, a member of a more derived trochid clade (27), the larval shell is not completely calcified at the time of torsion (26), and we suspect that it also may lack the rigidity required to produce torsion by muscle contraction.
Further investigations of torsion, both as a developmental event and as a key evolutionary innovation, require a phylogenetic context in which comparative morphogenesis is pursued at a much higher level of resolution. The phenomenon of torsion becomes more interesting if loose constraints on the evolution of development have indeed permitted the emergence of multiple morphogenetic pathways to a single, more tightly constrained body plan of the torted larva and adult gastropod.
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