Associations between shell morphology and land crab predation in the land snail Cerion

1. The land crab Gecarcinus lateralis is a significant predator of the abundant Bahamian land snails of the genus Cerion . The crabs typically 'scissor' the cylindrical shells in half or break the lip and peel back the shell to reach the animal which withdraws two or three whorls into the shell. Scars on shells of live adults at 73 sites in the Bahamas and Florida Keys show that about 8% (range: 0–44%) of the snails have survived attacks of this type.
2. An artificial crab claw was used to investigate the compressive force required to break Cerion shells of different morphotypes. Defining shell strength as the ability to withstand compressive forces, 10 morphotypes were found that exhibited mean relative strengths of between 30 and 300 newtons. Feeding trials with one adult crab showed that snails whose shells could withstand compressive forces of > 95 N were safe from this individual predator.
3. Multiple linear regression analyses showed that both shell size (length and width) and shell wall thickness were the ultimate determinants of shell strength. Ribs strengthen the shell by contributing to wall thickness and also by increasing overall shell width. The thickened adult shell lip and collabral ribs provide effective protection from attack by peeling.     

A DEVELOPMENTAL CONSTRAINT IN CERION,WITH COMMENTS ON THE DEFINITION AND INTERPRETATION OF CONSTRAINT IN EVOLUTION

Since orthodox evolutionary theory is functionalist, constraints attain their most important positive meaning as channels of change imposed by historical and formal determinants, rather than by immediate natural selection. Since ontogeny is the usual locus of expression for these determinants, developmental constraint is an appropriate, general term. A particular developmental constraint in Cerion, most variable of West Indian land snails, stands out for two reasons: 1) it is simply and inexorably defined as a consequence both of formal principles (coiling of tube about axis) and of historical contingencies in Cerion's invariant allometry of growth; 2) it is pervasive in its influence, underlying major patterns of variation in every Cerion study I have ever undertaken. I refer to this pattern as the “jigsaw constraint.” When whorls are large and final size is limited, adult shells must grow fewer whorls. In Cerion, this obvious fact is promoted from trivial to important because complex allometries impose a substantial set of further consequences for form upon this basic trade-off of whorl size and whorl number. I show that this complex of consequences dominates patterns of natural variation in Cerion at all levels (among shells within samples, between samples in the geographic variation of single species, and between species in multitaxon faunas). It also sets patterns of hybridization between taxa. This paper is primarily a compendium of such examples. It is designed to illustrate the importance of this constraint by the fundamental criterion of relative frequency.     

Three-dimensional geometric morphometric analysis of the humerus: Comparative postweaning ontogeny between fossorial and semiaquatic water voles (Arvicola)

Different types of locomotion in phylogenetically close rodent species can lead to significantly different growth patterns of certain skeletal structures. In the present study, we compared the allometric and phenotypic trajectories of the humerus in semiaquatic (Arvicola sapidus) and fossorial (Arvicola scherman) water vole taxa, using three-dimensional geometric morphometrics, to investigate the relationships between functional and ontogenetic differences. Results revealed shared humerus traits between A. sapidus and A. scherman, specifically an expansion of the epicondylar and deltopectoral crests along postnatal ontogeny. In both species, the humerus of young specimens is more robust than in adults, possibly as a compensatory response for lower bone stiffness. However, significant interspecific differences were detected in all components of allometric and phenotypic trajectories. Noticeably divergent allometric trajectories were observed, probably as a result of different functional pressures exerted on this bone. Important differences in the form of the adult humerus between taxa were also found, particularly in features located in muscle insertion zones. Furthermore, the allometric regression revealed certain shape variation not associated with size in A. scherman, suggesting mechanical stress produced by the persistent digging activity during adulthood. A. scherman is a chisel-tooth digger that shares several traits in the humerus morphology with scratch-digger rodent species. Nevertheless, these shared characteristics are less pronounced in fossorial water voles, which is congruent with the different implications of the forelimb in the digging activity in these two types of diggers.     

Morphological development and allometric growth patterns in hatchery-reared California halibut larvae

Morphological development, allometric growth and behaviour of hatchery-reared California halibut Paralichthys californicus were studied from hatching to metamorphosis (42 days post hatch, dph) at 187° C. Mean standard length ( L _S) of larvae and juveniles increased from 2.1 mm at hatching to 10.5 mm at metamorphosis with the increase in length being approximately linear. Stages of morphological development were described using the alphabetic staging (A–I) used for other flatfish species. Organogenesis and differentiation were more rapid and complex in yolk-sac (hatching, stage A–3 dph, stage B), preflexion (3–19 dph, stages B–C), and flexion larvae (from 20 to 23 dph, stages D–E), as larvae developed most of their sensory, feeding, respiratory and swimming systems. After notochord flexion at 24–25 dph (stage F), most morphological changes were related to the progressive transformation from a bilateral symmetrical larva to an asymmetrical benthic juvenile (42 dph, stages G–I).     

On the development, habitat selection and taxonomy of Helix (Jacosta) siphnica Kobelt (Gastropoda, Helicellinae)

The environmental factors affecting the distribution, variation, and development and taxonomy of Helix (Jacosta) siphnica Kobelt, 1883, an endemic landsnail of Siphnos Island (Cyclades, Greece), are examined.
Two types of populations can be distinguished due to different strategies of shell development. In the first, and more frequent, type, the keeled and depressed juvenile shells, become rounded in the later developmental stages. In the second type, in all developmental stages, only keeled shells are found. In this study changes in the allometric relationships of shell height, shell diameter and whorls are correlated with the development of the genital system and changes in habitat selection. The keeled forms are found in drier and more stony environments. The degradation of the forests to dry maquis and frygana and desertification in the Aegean insular ecosystems are probably connected with the development of keeled forms. Keeled populations of Trochoidea siphnica are regarded as an example of neoteny leading to paedomorphosis by retardation.     

GEOGRAPHIC VARIATION AND HETEROCHRONY IN TWO SPECIES OF COWRIES (GENUS CYPRAEA)

Geographic variation in the marine, Indo-Pacific cowry, Cypraea caputserpentis, involves clinal variations that parallel the ontogenetic development of adult shell characteristics. Cypraea caputdraconis, a closely related species endemic to Easter Island and Sala y Gómez, is morphologically similar to juvenile C. caputserpentis. Using multivariate measures of size and shape, I examine these patterns as a possible outcome of heterochrony, or changes in the timing of developmental events in ontogeny. Whorl-expansion rates of juvenile shells are significantly higher in C. caputdraconis when compared to C. caputserpentis and are negatively correlated with surface seawater temperatures among populations of C caputserpentis. High expansion rates, often associated with slow growth, result in a delay in the onset of lateral callus development and subsequent paedomorphosis. Ontogenetic trajectories calculated from growth series of adult and preadult shells indicate that paedomorphosis results from the combined effects of neoteny and post-displacement. Paedomorphosis among cowries may result from the advantages of larger body size relative to shell size under reduced predation intensities and associated increases in fecundity.     

The Gavialis-Tomistoma debate: the contribution of skull ontogenetic allometry and growth trajectories to the study of crocodylian relationships

The phylogenetic placement of Tomistoma and Gavialis crocodiles depends largely upon whether molecular or morphological data are utilized. Molecular analyses consider them as sister taxa, whereas morphological/paleontological analyses set Gavialis apart from Tomistoma and other crocodylian species. Here skull allometric trajectories of Tomistoma and Gavialis were contrasted with those of two longirostral crocodylian taxa, Crocodylus acutus and Mecistops cataphractus, to examine similarities in growth trajectories in light of this phylogenetic controversy. Entire skull shape and its two main modules, rostrum and postrostrum, were analyzed separately. We tested differences for both multivariate angles between trajectories and for shape differences at early and late stages of development. Based on a multivariate regression of shape data and size, Tomistoma seems to possess a peculiar rate of growth in comparison to the remaining taxa. However, its morphology at both juvenile and adult sizes is always closer to those of Brevirostres crocodylians, for the entire head shape, as well as the shape of the postrostrum and rostrum. By contrast, the allometric trajectory of Gavialis always begins and ends in a unique region of the multidimensional morphospace. These findings concur with a morphological hypothesis that places Gavialis separate from Brevirostres, and Tomistoma closer to other crocodylids, and provides an additional, and independent, data set to inform on this ongoing phylogenetic discussion.     

Cranial ontogeny in Stegoceras validum (Dinosauria: Pachycephalosauria): a quantitative model of pachycephalosaur dome growth and variation

Historically, studies of pachycephalosaurs have recognized plesiomorphically flat-headed taxa and apomorphically domed taxa. More recently, it has been suggested that the expression of the frontoparietal dome is ontogenetic and derived from a flat-headed juvenile morphology. However, strong evidence to support this hypothesis has been lacking. Here we test this hypothesis in a large, stratigraphically constrained sample of specimens assigned to Stegoceras validum, the best known pachycephalosaur, using multiple independent lines of evidence including conserved morphology of ornamentation, landmark-based allometric analyses of frontoparietal shape, and cranial bone histology. New specimens show that the diagnostic ornamentation of the parietosquamosal bar is conserved throughout the size range of the sample, which links flat-headed specimens to domed S. validum. High-resolution CT scans of three frontoparietals reveal that vascularity decreases with size and document a pattern that is consistent with previously proposed histological changes during growth. Furthermore, aspects of dome shape and size are strongly correlated and indicative of ontogenetic growth. These results are complementary and strongly support the hypothesis that the sample represents a growth series of a single taxon. Cranial dome growth is positively allometric, proceeds from a flat-headed to a domed state, and confirms the synonymy of Ornatotholus browni as a juvenile Stegoceras. This dataset serves as the first detailed model of growth and variation in a pachycephalosaur. Flat-headed juveniles possess three characters (externally open cranial sutures, tuberculate dorsal surface texture, and open supratemporal fenestrae) that are reduced or eliminated during ontogeny. These characters also occur in putative flat-headed taxa, suggesting that they may also represent juveniles of domed taxa. However, open cranial sutures and supratemporal fenestrae are plesiomorphic within Ornithischia, and thus should be expected in the adult stage of a primitive pachycephalosaur. Additional lines of evidence will be needed to resolve the taxonomic validity of flat-headed pachycephalosaur taxa.     

Post-weaning cranial ontogeny in two bandicoots (Mammalia,Peramelomorphia, Peramelidae) and comparison with carnivorous marsupials

The ontogeny of the skull has been studied in several marsupial groups such as didelphids, microbiotheriids, and dasyurids. Here, we describe and compare the post-weaning ontogeny of the skull in two species of bandicoots, Echymipera kalubu (Echymiperinae) and Isoodon macrourus (Peramelinae), analyzing specific allometric trends in both groups, describing common (and specific) patterns, and discussing them on functional and phylogenetic grounds. Growth patterns were analyzed both qualitatively and quantitatively, including bivariate and multivariate analyses of allometry. We also evaluated character transformation and phylogenetic signals of the allometric patterns in several groups of marsupials and some placentals. We identified morphological changes between juvenile and adult stages in both species of peramelids, many related to the development of the trophic apparatus. Notable differences were detected in the patterns of growth, suggesting divergences in ontogenetic trajectories between both species. Both bivariate and multivariate methods indicate that positive allometries in E. kalubu apply to longitudinal dimensions, whereas in I. macrourus, positive allometries are restricted to vertical dimensions of the skull. The comparison of the allometric trends of two bandicoots with previously studied taxa reveals that although peramelids exhibit a particularly short gestation period and divergent morphology compared to other marsupials, their pattern does not show any particular trend. Some allometric trends seem to be highly conserved among the species studied, showing weak phylogenetic signal. Marsupials in general do not show particular patterns of post-weaning skull growth compared with placentals.     

A developmental transition in growth control during zebrafish caudal fin development

A long-standing question in developmental biology is how do growing and developing animals achieve form and then maintain it. We have revealed a critical transition in growth control during zebrafish caudal fin development, wherein a switch from allometric to isometric growth occurs. This morphological transition led us to hypothesize additional physiological changes in growth control pathways. To test this, we fasted juvenile and adult zebrafish. Juvenile fins continued allometric growth until development of the mature bi-lobed shape was completed. In contrast, the isometric growth of mature adult fins arrested within days of initiating a fast. We explored the biochemical basis of this difference in physiology between the two phases by assessing the sensitivity to rapamycin, a drug that blocks a nutrient-sensing pathway. We show that the nutrition-independent, allometric growth phase is resistant to rapamycin at 10-fold higher concentrations than are effective at arresting growth in the nutrition-dependent, isometric growth phase. We thus link a morphological transition in growth control between allometric and isometric growth mechanisms to different physiological responses to nutritional state of the animal and finally to different pharmacological responses to a drug (rapamycin) that affects the nutrition-sensing mechanism described from yeast to human.     

THE CONSEQUENCES OF BEING DIFFERENT: SINISTRAL COILING IN CERION

The overwhelming predominance of dextral coiling in gastropods is an outstanding and puzzling phenomenon. A few sinistral specimens (left coiling individuals) have been found in many dextral species. Only six sinistral shells have ever been found in Cerion; we base this analysis on the five available shells. We ask whether reversed symmetry is a simple either-or switch without further consequences for shell form, or whether sinistrality engenders associated effects, making left-coiling shells unlike their dextral deme-mates in other ways. All five sinistral shells differ in features of size and coiling late in growth, leading to relatively small apertures and a slight twist in the axis of coiling. We detect and measure this effect as follows: in multivariate morphospace, sinistrals occupy peripheral positions among their dextral deme-mates; in univariate analysis, sinistrals are consistently different for a set of characters involving covariance patterns never before seen in a decade of studies on ontogenetic and age-standardized variation in dextrals; a bootstrap procedure does not recover similar patterns in randomly constituted samples of dextrals matching the true sinistral distribution; direct x-ray measures of the coiling axis detect its slight twist in sinistrals. We discuss the implications of these unsuspected associations for the issues of developmental constraint upon the evolution of morphology.     

Continuous growth-line sequences in gastropod shells

Studies of gastropod shell growth at the level of fine growth layers are scarce, because coiling of gastropod shells hinders the observation of continuous growth series spanning across whorls. We propose here a new method to obtain continuous growth patterns of gastropod shells over whorls with Terebralia palustris (L.) as an example. Comparison of vertical and horizontal sections of the shell of this species reveals that growth patterns can be observed continuously for several whorls on the vertical section of the columella. In addition, an obvious tidal growth pattern preserved in this species enables us to trace its growth with a precision of 12.4 h and indicates that it takes about two years for a shell to grow from 3 cm to 9.5 cm in height and add 5 complete whorls.     

Metamorphosis and evolution of feeding behaviour in salamanders of the family Plethodontidae

Plethodontid salamanders capture prey with enhanced tongue protraction relative to other salamander taxa, yet metamorphosing plethodontids are hypothesized to be constrained relative to direct-developing plethodontids in their degree of tongue evolution (protraction length and velocity) by the presence of a larval stage in development. In this biphasic life history the hyobranchial apparatus serves the conflicting functions of larval suction feeding and adult tongue protraction. The deletion of the larval stage removes one of the conflicting functions and has thus permitted direct-developing plethodontids to circumvent this constraint and evolve extremely long tongues, which in some species can be projected to 80% of body length. To evaluate this constraint hypothesis and explore taxonomic diversity of feeding behaviours, we studied feeding in larvae, adults and metamorphosing individuals of seven species of metamorphosing plethodontids from the basal taxa Desmognathinae and Hemidactyliini using direct observations, high-speed videography and kinematic analysis. We found that larval plethodontids suction feed, but feeding is suspended entirely during metamorphosis, and aquatic adults do not suction feed. Adults have exapted the terrestrial modes of tongue and jaw prehension for aquatic prey capture. These findings substantiate the premise that suction feeding and tongue protraction are conflicting functions, and thus our results support the constraint hypothesis. Plethodontid adults have evolved their extreme tongue protraction ability at the expense of adult suction feeding. The rapid metamorphosis that characterizes plethodontids may be an adaptation that minimizes the non-feeding period imposed by the evolution of derived tongue protraction in adults. © 2002 The Linnean Society of London, Zoological Journal of the Linnean Society , 2002, 134 , 375–400.     

The interaction of temperature and fish size on growth of juvenile turbot

Growth rate of tagged juvenile turbot was significantly influenced by the interaction of temperature and fish size. The results suggest the optimum temperature for growth of juvenile turbot in the size range 25–75 g is between 16 and 19°C. Optimal temperature for growth decreased rapidly with increasing size, and is between 13 and 16°C for 100 g turbot. Although individual growth rates varied highly at all times within the temperature treatments, significant size rank correlations were maintained during the experimental period. The study confirms that turbot exhibit ontogenetic variation in temperature optimum, which might partly explain different spatial distribution of juvenile and adult turbot in ocean waters.     

Ontogenetic changes in the trochoidean (Archaeogastropoda) radula, with some phylogenetic interpretations

Radulae have been examined of juvenile specimens of 18 species belonging to the Turbinidae, the Tricoliidae. and 6 subfamilies of Trochidae. The investigations show that all species pass through profound changes, usually finishing at a size of 1.5–3 teleoconch whorls. Most species have an identical, shared morphology at a size of up to 1.5–2 teleoconch whorls, except the species of Calliostomatinac and Solariellinae. The evolutionary consequences are discussed and it is suggested that such an unspecialized starting point means a high potential for specializations and future evolution. For the taxonomist this means a reduction in the reliability of radular differences as a systematic tool.     

Extreme Cranial Ontogeny in the Upper Cretaceous Dinosaur Pachycephalosaurus

Background

Extended neoteny and late stage allometric growth increase morphological disparity between growth stages in at least some dinosaurs. Coupled with relatively low dinosaur density in the Upper Cretaceous of North America, ontogenetic transformational representatives are often difficult to distinguish. For example, many hadrosaurids previously reported to represent relatively small lambeosaurine species were demonstrated to be juveniles of the larger taxa. Marginocephalians (pachycephalosaurids + ceratopsids) undergo comparable and extreme cranial morphological change during ontogeny.

Methodology/Principal Findings

Cranial histology, morphology and computer tomography reveal patterns of internal skull development that show the purported diagnostic characters for the pachycephalosaurids Dracorex hogwartsia and Stygimoloch spinifer are ontogenetically derived features. Coronal histological sections of the frontoparietal dome of an adult Pachycephalosaurus wyomingensis reveal a dense structure composed of metaplastic bone with a variety of extremely fibrous and acellular tissue. Coronal histological sections and computer tomography of a skull and frontoparietal dome of Stygimoloch spinifer reveal an open intrafrontal suture indicative of a subadult stage of development. These dinosaurs employed metaplasia to rapidly grow and change the size and shape of their horns, cranial ornaments and frontoparietal domes, resulting in extreme cranial alterations during late stages of growth. We propose that Dracorex hogwartsia, Stygimoloch spinifer and Pachycephalosaurus wyomingensis are the same taxon and represent an ontogenetic series united by shared morphology and increasing skull length.

Conclusions/Significance

Dracorex hogwartsia (juvenile) and Stygimoloch spinifer (subadult) are reinterpreted as younger growth stages of Pachycephalosaurus wyomingensis (adult). This synonymy reduces the number of pachycephalosaurid taxa from the Upper Cretaceous of North America and demonstrates the importance of cranial ontogeny in evaluating dinosaur diversity and taxonomy. These growth stages reflect a continuum rather than specific developmental steps defined by “known” terminal morphologies.     

The development of the serpulid Pomatoleios kraussii (Annelida, Polychaeta)

The development of Pomatoleios kraussii is extremely similar to that of Pomatoceros triqueter , and is completed under laboratory conditions in 1–3 weeks at 25–27°C. Mature larvae settle and metamorphose preferentially on the shells of adult conspecifics.     

Effects of maternal investment on larvae and juveniles of the annelid Capitella teleta determined by experimental reduction of embryo energy content

Experimental manipulations of the energy content of marine invertebrate embryos have been useful in testing key assumptions of life history theory, especially those concerning relationships between egg size, length of the planktonic period, and juvenile size and quality. However, methods for such “allometric engineering” experiments have been available for only a limited set of taxa (those with regulative early development, e.g., cnidarians and echinoderms). Here, we describe a method for the reduction of embryo energy content in the spirally cleaving embryos of a marine annelid, Capitella teleta, by targeted deletion of endodermal precursor cells. Embryos of C. teleta in which up to three cells (the macromeres 3A, 3B, and 3C) were deleted formed morphologically normal lecithotrophic larvae that were much smaller than larvae developing from control embryos. Experimental larvae metamorphosed at high rates, forming juveniles that were smaller than control juveniles. Juveniles derived from treated embryos had functional midguts, ingested and digested food, and grew into sexually mature adults. These results are consistent with those from previous allometric engineering studies of echinoid echinoderms, which suggest that in facultatively planktotrophic or lecithotrophic species, little maternally derived energy is used for construction of the larval body; instead, the majority is allocated to the formation of a large, high‐quality juvenile. Cleavage programs are highly conserved among divergent spiralian taxa (e.g., molluscs, nemerteans, and platyhelminths), so this method will likely be applicable to a diverse set of embryos. Similar experiments carried out in these diverse taxa will be extremely useful for evaluating inferences on relationships between egg size, length of the planktonic period, and juvenile size and quality previously based only on experiments on echinoid echinoderms.     

Morphological Features of Supralittoral Mollusks of the Genus Cecina (Gastropoda: Pomatiopsidae) from Peter the Great Bay, Sea of Japan

Amphibious mollusks of the genus Cecina in the littoral and supralittoral of the Sea of Japan are represented by three species: Cecina manchurica A. Adams, 1861; C. tatarica (Schrenck, 1867); and C. scarlatoi Prozorova, 1996. Additional data on the morphology of the shell and radula are provided. Indices for the identification of adult decollated and corroded shells of these species which retained only 3.0–2.5 last whorls are proposed: (1) the ratio of the width of the ultimate whorl (without aperture) to the length of the ultimate and penultimate whorls and (2) the ratio of the width of the third whorl (from the bottom) to the width of the ultimate whorl (without aperture).     

Homoplasy and the evolution of ontogeny in papionin primates

Recent advances in developmental biology reveal that patterns of morphological development, even during early phases, may be highly susceptible to evolutionary change. Consequently, developmental data may be uninformative with regard to distinguishing homology and homoplasy. The present analysis evaluates postnatal ontogeny in papionin primates to test hypotheses about homology and homoplasy during later periods of development. Specifically, the analysis studies the allometric bases of craniometric resemblances among four papionin genera to test the hypothesis that homoplasy in adult cranial form, particularly of baboons (Papio) and mandrills (Mandrillus), is underwritten by divergent patterns of development. Bivariate and multivariate allometric analyses demonstrate that the developmental patterns in Papio baboons diverge markedly from ontogenetic allometric trajectories in other papionin species. The resemblances between Papio and Mandrillus (assuming that patterns of development in smaller papionins are ancestral) are largely consequences of perinatal increases in relative brain size in juvenile Papio. Postnatal growth to large size and strong negative allometry of neurocranial form results in shape similarities because developmental pathways for large papionin genera intersect. Analyses show that allometric data may not be particularly informative in revealing homoplasy. However, placed into proper phylogenetic context, such data illustrate derived patterns of development that may reflect critically important life-history or ontogenetic adaptations.