Teeth outside the mouth: The evolution and development of shark denticles

Vertebrate skin appendages are incredibly diverse. This diversity, which includes structures such as scales, feathers, and hair, likely evolved from a shared anatomical placode, suggesting broad conservation of the early development of these organs. Some of the earliest known skin appendages are dentine and enamel-rich tooth-like structures, collectively known as odontodes. These appendages evolved over 450 million years ago. Elasmobranchs (sharks, skates, and rays) have retained these ancient skin appendages in the form of both dermal denticles (scales) and oral teeth. Despite our knowledge of denticle function in adult sharks, our understanding of their development and morphogenesis is less advanced. Even though denticles in sharks appear structurally similar to oral teeth, there has been limited data directly comparing the molecular development of these distinct elements. Here, we chart the development of denticles in the embryonic small-spotted catshark (Scyliorhinus canicula) and characterize the expression of conserved genes known to mediate dental development. We find that shark denticle development shares a vast gene expression signature with developing teeth. However, denticles have restricted regenerative potential, as they lack a sox2+ stem cell niche associated with the maintenance of a dental lamina, an essential requirement for continuous tooth replacement. We compare developing denticles to other skin appendages, including both sensory skin appendages and avian feathers. This reveals that denticles are not only tooth-like in structure, but that they also share an ancient developmental gene set that is likely common to all epidermal appendages.     

Microstructural morphology in early dermal denticles of hammerhead sharks (Elasmobranchii: Sphyrnidae) and related taxa

Mello, W.C., de Carvalho, J.J., Brito, P.M.M. 2011. Microstructural morphology in early dermal denticles of hammerhead sharks (Elasmobranchii: Sphyrnidae) and related taxa. —Acta Zoologica (Stockholm) 00 : 1–7. This study uses scanning electron microscopies to investigate and describe the microstructural diversity of dermal denticles in the family Sphyrnidae, which comprises all living hammerhead shark species, comparing them to other related taxa (i.e. Carcharhinus dussumieri, Carcharhinus plumbeus, Carcharhinus acronotus, Rhizoprionodon acutus, Negaprion brevirostris and Hemigaleus microstoma). The results reveal that sphyrnids present noticeable microstructures in the dermal denticles, distinguishing them from the other related species investigated. Additionally, scale patterns are the same in three distinct body regions (i.e. cephalic, branchial and dorsal fin). Species of Sphyrnidae that reach bigger total lengths and that are widely distributed (i.e. Sphyrna lewini and Sphyrna mokarran) presented more, smaller and nearly hexagonal microstructures that do not cover the entire scale surface, unlike species reaching smaller sizes and restricted to coastal habits (i.e. Sphyrna tiburo, Sphyrna tudes, Sphyrna media and Eusphyra blochii). The sphyrnid scales are similar to R. acutus and C. dussumieri rather than to the other species, but it is not possible to identify the sphyrnid species only by scale features. It is clear that a similar morphology of scales is not necessarily related to similar life habits, and that they are candidates to provide new characters in phylogenetical studies among sphyrnids.     

New data on the systematics and interrelationships of sawfishes (Elasmobranchii, Batoidea, Pristiformes)

New characters based on the arrangement and morphology of dermal denticles show that sawfishes can be divided into two distinctive groups. The first group, comprising the knifetooth sawfish Anoxypristis cuspidata , is characterized by tricuspid denticles variably located on both dorsal and ventral parts of the body. The second group is represented by species of the genus Pristis , showing an uniform and homogenous dermal covering of monocuspidate denticles on both dorsal and ventral sides of the body and within the buccopharyngeal cavity. Pristis is further divided into two subgroups: the first comprises species with denticles lacking any keels and furrows (the smalltooth sawfish Pristis pectinata , the green sawfish Pristis zijsron and the dwarf sawfish Pristis clavata ); the second comprises species with denticles presenting keels and furrows well differentiated on their anterior part (the common sawfish Pristis pristis , the largetooth sawfish Pristis perotteti and the greattooth sawfish Pristis microdon ). This investigation of the dermal covering provides results which agree with studies that separate the same two species groups of Pristis on the basis of other morphological data.     

Scymnodon plunketi (Waite, 1910): a junior synonym of Scymnodon macracanthus (Regan, 1906) (Somniosidae: Elasmobranchii)

The taxonomic status and validity of Scymnodon macracanthus (Regan, 1906) and Scymnodon plunketi (Waite, 1910) are revised in light of new material from the Southern Pacific and Indian Oceans. Despite being historically accepted as distinct taxa, recent studies suggested the possibility that these species could represent a single taxon. Morphometrics, meristics and morphology of dermal denticles show that S. plunketi is indeed a junior synonym of S. macracanthus. Previous distinctive characters proved to be the result of intraspecific variation. S. macracanthus is therefore redescribed including an updated comparative diagnosis for the genus Scymnodon in the family Somniosidae.     

The relationships of Gasteroclupea branisai Signeux, 1964, a freshwater double-armored herring (Clupeomorpha,Ellimmichthyiformes) from the Late Cretaceous-Paleocene of South America

The clupeomorph fish Gasteroclupea branisai Signeux, 1964 from the Late Cretaceous-Paleocene of El Molino Formation, Cayara locality, Bolivia is redescribed in detail. This South American double-armored herring is the sole member of the family Gasteroclupeidae and exhibits a unique combination of features (skull roof ornamented with fine tubercles, beryciform foramen, endopterygoid teeth, about 16–18 supraneurals, a series of 35–38 predorsal and 40 ventral scutes, median fins small and containing 12–14 rays) that clearly supports its assignment to the extinct clupeomorph order Ellimmichthyiformes. G. branisai shares a number of synapomorphies with Sorbinichthys elusivo and S. africanus (five hypurals, second hypural autogenous, distal end of the second uroneural not reaching the distal end of the first uroneural) with which it forms a monophyletic assemblage recognized herein for the first time as the new suborder Sorbinichthyoidei. The peculiar morphology of Gasteroclupea that is characterized by having an extremely deep abdominal profile, hypertrophied coracoid, and elongated pectoral fins, resembles in many aspects the body plan of extant freshwater hatchetfishes of the characiform family Gasteropelecidae, suggesting that the morphological adaptations of G. branisai can be related, at least in part, to a similar lifestyle.     

An insight into the skin glands,dermal scales and secretions of the caecilian amphibian Ichthyophis beddomei

The caecilian amphibians are richly endowed with cutaneous glands, which produce secretory materials that facilitate survival in the hostile subterranean environment. Although India has a fairly abundant distribution of caecilians, there are only very few studies on their skin and secretion. In this background, the skin of Ichthyophis beddomei from the Western Ghats of Kerala, India, was subjected to light and electron microscopic analyses. There are two types of dermal glands, mucous and granular. The mucous gland has a lumen, which is packed with a mucous. The mucous-producing cells are located around the lumen. In the granular gland, a lumen is absent; the bloated secretory cells, filling the gland, are densely packed with granules of different sizes which are elegantly revealed in TEM. There is a lining of myo-epithelial cells in the peripheral regions of the glands. Small flat disk-like dermal scales, dense with squamulae, are embedded in pockets in the dermis, distributed among the cutaneous glands. 1–4 scales of various sizes are present in each scale pocket. Scanning electron microscopic observation of the skin surface revealed numerous glandular openings. The skin gland secretions, exuded through the pores, contain fatty acids, alcohols, steroid, hydrocarbons, terpene, aldehyde and a few unknown compounds.     

Morphological variations in a tooth family through ontogeny in Pleurodeles waltl (Lissamphibia, Caudata)

Most nonmammalian species replace their teeth continuously (so-called polyphyodonty), which allows morphological and structural modifications to occur during ontogeny. We have chosen Pleurodeles waltl, a salamander easy to rear in the laboratory, as a model species to establish the morphological foundations necessary for future molecular approaches aiming to understand not only molecular processes involved in tooth development and replacement, but also their changes, notably during metamorphosis, that might usefully inform studies of modifications of tooth morphology during evolution. In order to determine when (in which developmental stage) and how (progressively or suddenly) tooth modifications take place during ontogeny, we concentrated our observations on a single tooth family, located at position I, closest to the symphysis on the left lower jaw. We monitored the development and replacement of the six first teeth in a large growth series ranging from 10-day-old embryos (tooth I1) to adult specimens (tooth I6), using light (LM), scanning (SEM), and transmission electron (TEM) microscopy. A timetable of the developmental and functional period is provided for the six teeth, and tooth development is compared in larvae and young adults. In P. waltl the first functional tooth is not replaced when the second generation tooth forms, in contrast to what occurs for the later generation teeth, leading to the presence of two functional teeth in a single position during the first 2 months of life. Larval tooth I1 shows dramatically different features when compared to adult tooth I6: a dividing zone has appeared between the dentin cone and the pedicel; the pulp cavity has enlarged, allowing accommodation of large blood vessels; the odontoblasts are well organized along the dentin surface; tubules have appeared in the dentin; and teeth have become bicuspidate. Most of these modifications take place progressively from one tooth generation to the next, but the change from monocuspid to bicuspid tooth occurs during the tooth I3 to tooth I4 transition at metamorphosis.     

Structure and development of the ctenial spines on the scales of a teleost fish,the cichlid Cichlasoma nigrofasciatum

Sire, J.‐Y. and Arnulf, I. 2000. Structure and development of the ctenial spines on the scales of a teleost fish, the cichlid Cichlasoma nigrofasciatum. — Acta Zoologica (Stockholm) 81 : 139–158 Numerous teleost species possess ctenoid scales characterized by the presence of ctenial spines arranged in rows (the cteni) along their posterior, free margin. Whilst the morphology and function of the ctenial spines are similar to those of odontodes (extra‐oral teeth), e.g. in armored catfish, their homology is questionable. To address this problem, we have studied ctenial spine development, structure, attachment to a bony support, and replacement with the aim of comparing these features to those described for odontodes. The ctenial spines have been studied in a growth series of the cichlid Cichlasoma nigrofasciatum, using light, scanning and transmission electron microscopy. Ctenial spines are entirely constituted of a collagen matrix. They lack a pulp cavity and, although their distal end can be in contact with the epidermal basal layer cells, they are not covered by an enameloid‐like tissue. They are attached to the scale by means of a narrow strand of unmineralized collagen matrix acting as a ligament and allowing spines to be movable. The ctenial spines develop as prolongations of the external layer of the scale, a woven‐fibroid collagen matrix, and subsequently grow by addition of parallel‐fibred collagen matrix. New ctenial spines are added at the posterior scale border in waves that follow the same rhythm as the deposition of circuli in the anterior region. From the focus region to the scale border, the ctenial spines constitute lines in which only the most posterior ctenial spine is functional. The other spines that are no longer functional are not shed but resorbed from the top, and their attachment region mineralizes and thickens by deposition of new material. The remnants of spines constitute the main part of the superficial layer of the scale in which anchoring bundles attach; this region is covered afterwards by the limiting layer, a tissue devoid of collagen fibrils. Because of their tooth‐like morphology (shape and size), their posterior orientation and their attachment to the scale surface, the ctenial spines resemble odontodes. Moreover, both elements perform a similar hydrodynamic function. Nevertheless, the structure and development of the ctenial spines differ completely from those of odontodes and consequently, they cannot be considered homologous elements. Ctenial spines and odontodes in teleosts provide us with a beautiful example of homoplasy; they share shape and function, but have a different origin as evidenced by their different structure and process of development.     

Morphology and mechanics of the teeth and jaws of white-spotted bamboo sharks (Chiloscyllium plagiosum)

The teeth of white-spotted bamboo sharks (Chiloscyllium plagiosum) are used to clutch soft-bodied prey and crush hard prey; however, the dual function is not evident from tooth morphology alone. Teeth exhibit characteristics that are in agreement with a clutching-type tooth morphology that is well suited for grasping and holding soft-bodied prey, but not for crushing hard prey. The dual role of this single tooth morphology is facilitated by features of the dental ligament and jaw joint. Tooth attachment is flexible and elastic, allowing movement in both sagittal and frontal planes. During prey capture spike-like tooth cusps pierce the flesh of soft prey, thereby preventing escape. When processing prey harder than the teeth can pierce the teeth passively depress, rotating inward towards the oral cavity such that the broader labial faces of the teeth are nearly parallel to the surface of the jaws and form a crushing surface. Movement into the depressed position increases the tooth surface area contacting prey and decreases the total stress applied to the tooth, thereby decreasing the risk of structural failure. This action is aided by a jaw joint that is ventrally offset from the occlusal planes of the jaws. The offset joint position allows many teeth to contact prey simultaneously and orients force vectors at contact points between the jaws and prey in a manner that shears or rolls prey between the jaws during a bite, thus, aiding in processing while reducing forward slip of hard prey from the mouth. Together the teeth, dental ligament, and jaws form an integrated system that may be beneficial to the feeding ecology of C. plagiosum, allowing for a diet that includes prey of varying hardness and elusiveness.     

The distribution and evolution of exocrine compound glands in Erotylinae (Insecta: Coleoptera: Erotylidae)

Summary. Members of the family Erotylidae and especially of the subfamily Erotylinae possess a whole arsenal of compound integumentary glands. Their external pores are located in several parts of the body, mainly in the corners and along the lateral margins of the pronotum, beside the compound eyes (periocular glands), on the subgenal braces (subocular glands), on the abdominal ventrites, and more rarely on the prosternal and mesoventral intercoxal processes, the mentum and the mandibles. To evaluate the evolution of the various exocrine glands their occurrence is described for 55 species of Erotylidae (including the former Languriidae), and data from the literature are included for nine further species and two subfamilies. In some phylogenetically crucial cases, the glandular nature was verified by internal inspection (search for glandular ducts), and in some critical species or genera an extended sample was studied. Gland characters and their phylogenetic implications are discussed and mapped on a previously published erotylid phylogeny.

Résumé. La distribution et l’évolution des glandes exocrines composées chez les Erotylinae (Insecta: Coleoptera: Erotylidae). Les membres de la famille des Erotylidae et spécialement de la sous-famille des Erotylinae ont un large arsenal de glandes tégumentaire composées. Leurs pores externes sont situés dans différentes parties du corps, surtout dans les coins et les bords des marges latérales du pronotum, à côté des yeux composés (glandes péri-oculaires), sur les ventrites abdominaux, et plus rarement sur les processus prosternaux intercoxal et mésoventral, le mentum et les mandibules. Pour évaluer l’évolution des différentes glandes exocrines, leur occurrence est décrite pour 55 espèces d'Erotylidae (y compris les anciens Languriidae), tandis que des données de la littérature sont incluses pour 9 espèces supplémentaires et 2 sous-familles. Dans certains cas phylogénétiquement cruciaux, la nature glandulaire a été vérifiée par un examen interne (recherche de canaux glandulaires). L’échantillonnage a été étendu pour certaines espèces ou certains genres critiques. Les caractères des glandes et leurs implications phylogénétiques sont discutées et cartographiées à partir d'une phylogénie des Erotylidae précédemment parue.     

Scale morphology and flexibility in the shortfin mako Isurus oxyrinchus and the blacktip shark Carcharhinus limbatus

We quantified placoid scale morphology and flexibility in the shortfin mako Isurus oxyrinchus and the blacktip shark Carcharhinus limbatus. The shortfin mako shark has shorter scales than the blacktip shark. The majority of the shortfin mako shark scales have three longitudinal riblets with narrow spacing and shallow grooves. In comparison, the blacktip shark scales have five to seven longitudinal riblets with wider spacing and deeper grooves. Manual manipulation of the scales at 16 regions on the body and fins revealed a range of scale flexibility, from regions of nonerectable scales such as on the leading edge of the fins to highly erectable scales along the flank of the shortfin mako shark body. The flank scales of the shortfin mako shark can be erected to a greater angle than the flank scales of the blacktip shark. The shortfin mako shark has a region of highly flexible scales on the lateral flank that can be erected to at least 50°. The scales of the two species are anchored in the stratum laxum of the dermis. The attachment fibers of the scales in both species appear to be almost exclusively collagen, with elastin fibers visible in the stratum laxum of both species. The most erectable scales of the shortfin mako shark have long crowns and relatively short bases that are wider than long. The combination of a long crown length to short base length facilitates pivoting of the scales. Erection of flank scales and resulting drag reduction is hypothesized to be passively driven by localized flow patterns over the skin. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

Biological characterization of the skin of shortfin mako shark Isurus oxyrinchus and preliminary study of the hydrodynamic behaviour through computational fluid dynamics

This study characterized the morphology, density and orientation of the dermal denticles along the body of a shortfin mako shark Isurus oxyrinchus and identified the hydrodynamic parameters of its body through a computational fluid‐dynamics model. The study showed a great variability in the morphology, size, shape, orientation and density of dermal denticles along the body of I. oxyrinchus. There was a significant higher density in dorsal and ventral areas of the body and their highest angular deviations were found in the lower part of the mouth and in the areas between the pre‐caudal pit and the second dorsal and pelvic fins. A detailed three‐dimensional geometry from a scanned body of a shark was carried out to evaluate the hydrodynamic properties such as drag coefficient, lift coefficient and superficial (skin) friction coefficient of the skin together with flow velocity field, according to different roughness coefficients simulating the effect of the dermal denticles. This preliminary approach contributed to detailed information of the denticle interactions. As the height of the denticles was increased, flow velocity and the effect of lift decreased whereas drag increased. The highest peaks of skin friction coefficient were observed around the pectoral fins.     

Structure and development of first-generation teeth in the cichlid Hemichromis bimaculatus (Teleostei, Cichlidae)

In order to build a reference system to assess results of ongoing in vitro experiments on the study of epithelial-mesenchymal interactions during odontogenesis in actinopterygians, we have chosen to study the first-generation teeth of the cichlid Hemichromis bimaculatus from initiation until attachment both at the light and transmission electron microscopical level. Although their development follows the general pattern of teleost tooth formation, first-generation teeth show peculiarities compared with later tooth generations, including their size, bare emergence from the epithelium, absence of dentinal tubules and of nerves and capillaries in the pulp cavity, and organization of the outer dental epithelium. Four developmental stages (a to d) prior to attachment (stage e) have been distinguished. The oral epithelium invaginates into the underlying mesenchyme (stage a) and is later folded to form a bell-shaped dental organ (stage b) without any primordial thickening, or any other morphological indication of imminent invagination. Then, the collagenous enameloid matrix is laid down, most probably by the odontoblasts (early stage c), soon followed by predentine deposition and the beginning of enameloid mineralization (late stage c). With ongoing dentinogenesis, the enameloid matrix matures (stage d), i.e. the organic constituents are removed and the matrix further mineralizes. Finally (stage e), an annular collar of attachment bone is deposited to fix the tooth onto the underlying bone.     

Spore ultrastructural features and significance of their diverse ornamental elements in the evolutionary history of the order Trichiales (Myxomycetes,Amoebozoa)

Spores are the dispersal and reproductive units in Myxomycetes, and their ornamentation, usually at the light microscopy resolution limit, is taxonomically meaningful. Here, we analyze with scanning and transmission electron microscopy the spore ultrastructural features in Trichiales, one of the most morphologically diverse orders. In Trichiales, the spore wall consists of two layers, an outer one, including the ornamentation, and an inner layer subdivided into two sections. The diversity of ornamental elements includes verrucae, bacula, pila, muri, and cristae, the two latter creating reticulate patterns. Each of these elements defines a broadly recognized ornamentation type except cristae, from which we differentiate for the first time the cristate reticulate and patched subtypes. Besides, our results point out a previous incorrect classification of the spores of the species Trichia decipiens and T. scabra. Advances in Trichiales phylogeny showed that the capillitium ornamental elements, such as the spirals, do not reflect phylogenetic relationships among the species. The same seems to apply to some of spore ornamentation types, e.g., baculate. Consequently, we may consider the need to combine multiple characters, like the spore and capillitium ornamentation, so that Trichiales systematics better reflect the still cryptic phylogenetic affinities.     

Peculiar Epibionts in Euplotidium itoi (Ciliata, Hypotrichida)

ABSTRACT. Euplotidium itoi share with some other species of the same genus a peculiar feature: the presence of a band of particles running along the right and left borders of the cell body and forming a sort of "scarf" at the dorsal anterior end. The ultrastructural analysis, here performed, revealed that these particles (reported in the literature as extrusomes) are always external to the cell and are inserted in matching depressions on the euplotidium cortex. They are present in two different forms: type I, whose ultrastructure recalls that of bacteria, are able to reproduce by binary fission; type II are not able to divide and contain peculiar structures (a granular dome-shaped zone, a complex extrusive apparatus and a network of regularly arranged fibrils) which render them more complicated with respect to the majority of prokaryotic organisms. These observations, together with the finding that these particles contain DNA, indicate that we are dealing with epibionts, that will be referred to as "epixenosomes" (ecto-organisms), rather than extrusomes. Some ideas about the nature of "epixenosomes" and their relationship with the host cell are proposed and discussed.     

General descriptions of the dermis structure of a juvenile whale shark Rhincodon typus from the Gulf of California

The aim of this study is to provide preliminary observations on the microanatomy of Rhincodon typus skin using histology and electron microscopy analyses. Skin biopsies were obtained from a deceased juvenile male shark (548 cm total length) stranded in La Paz, Mexico, during February 2018. The results of this study evidenced the basic structure of the dermal denticles in the epidermis of the trunk of the shark, as well as the composition of the connective tissue in the hypodermis. Histological images of the hypodermis showed a high concentration of collagen fibres, formed by a large number of fine and wavy fibres of compact shape and little intercellular substance.     

Study by transmission and scanning electron microscopy of the morphogenesis of three types of lingual papillae in the albino rat (Rattus rattus)

El‐Bakry, A.M. 2010. Study by transmission and scanning electron microscopy of the morphogenesis of three types of lingual papillae in the albino rat (Rattus rattus).—Acta Zoologica (Stockholm) 91 : 267–278 Tongues were removed from albino rat foetus on days 12 (E12) and 16 (E16) of gestation and from newborns (P0) and from juvenile rats on days 7 (P7), 14 (P14) and 21 (P21) postnatally for investigation by light, scanning, and transmission electron microscopy. Significant changes appeared during the morphogenesis of the papillae. At E12, two rows of rudiments of fungiform papillae were extended bilaterally on the anterior half of the tongue. At E16, the rudiments of fungiform papillae were regularly arranged in a lattice‐like pattern. A rudiment of circumvallate papillae could be recognized. No rudiment of filiform papillae was visible. No evidence of keratinization was recognizable. At P0, rudiments of filiform papillae were visible but had a more rounded appearance, with keratinization. The fungiform and circumvallate papillae were large and their outlines were somewhat irregular as that found in the adult rat. At P7, the filiform papillae were large and slender. The fungiform papillae became large and the shape of circumvallate papillae was almost similar to that observed in the adult. At P14 and P21, the shape and structure of the three types of papillae were irregular as those found in the adult. In conclusion, the rudiments of the fungiform and circumvallate papillae were visible earlier than those of the filiform papillae. The morphogenesis of filiform papillae advanced in a parallel manner with the keratinization of the lingual epithelium, in the period from just before birth to a few weeks after birth.     

Morphology and evolution of the cynipoid egg (Hymenoptera)

We describe gross egg morphology and provide the first data on eggshell ultrastructure in cynipoids (Hymenoptera) based on species representing three distinctly different life histories: internal parasitoids of endopterygote larvae, gall inducers and phytophagous inquilines (guests in galls). We then use existing phylogenetic hypotheses to identify putative changes in egg structure associated with evolutionary life-history transitions. We find four major structural changes associated with the shift from parasitoids laying their eggs inside a host larva to gall inducers laying their eggs in or on plants: (1) from a narrow and gradually tapering gross form to a distinct division into a stout body and a long and thin stalk; (2) from a thin to a thick eggshell; (3) from a flexible to a rigid endochorion; and (4) from crystal bundles with shifting orientation in the exochorion to layers of parallel crystal rods. By contrast, we find no major changes in egg structure associated with the transition from gall inducers to inquilines. Comparison between pre- and post-oviposition eggs of one gall inducer and one inquiline suggests that mechanical stress during the passage through the egg canal gives rise to numerous tiny stress fractures in the boundary separating the exo- and endochorion. In one of the gall inducers, Diplolepis rosae , that end of the egg, which is inserted into the plant, has a specialized and apparently porous shell that may permit chemical exchange between the embryo and the plant. Other structures that could facilitate chemical communication with the host plant through the eggshell were, however, not observed in the eggs of gall inhabitants.  © 2003 The Linnean Society of London, Zoological Journal of the Linnean Society , 2003, 139 , 247–260.