Ectoderm,endoderm, and the evolution of heterodont dentitions

Mammalian dentitions consist of different shapes/types of teeth that are positioned in different regions of the jaw (heterodont) whereas in many fish and reptiles all teeth are of similar type (homodont). The process by which heterodont dentitions have evolved in mammals is not understood. In many teleosts teeth develop in the pharynx from endoderm (endodermal teeth), whereas mammalian teeth develop from the oral ectoderm indicating that teeth can develop (and thus possibly evolve) via different mechanisms. In this article, we compare the molecular characteristics of pharyngeal/foregut endoderm with the molecular characteristics of oral ectoderm during mouse development. The expression domains of Claudin6, Hnf3β, α‐fetoprotein, Rbm35a, and Sox2 in the embryonic endoderm have boundaries overlapping the molar tooth‐forming region, but not the incisor region in the oral ectoderm. These results suggest that molar teeth (but not incisors) develop from epithelium that shares molecular characteristics with pharyngeal endoderm. This opens the possibility that the two different theories proposed for the evolution of teeth may both be correct. Multicuspid (eg. molars) having evolved from the externalization of endodermal teeth into the oral cavity and monocuspid (eg. incisors) having evolved from internalization of ectodermal armour odontodes of ancient fishes. The two different mechanisms of tooth development may have provided the developmental and genetic diversity on which evolution has acted to produce heterodont dentitions in mammals. genesis 48:382–389, 2010. © 2010 Wiley‐Liss, Inc.     

Hypobranchial placodes in<Emphasis Type="Italic"> Xenopus laevis</Emphasis> give rise to hypobranchial ganglia,a novel type of cranial ganglia

Recently, a novel type of neurogenic placode was described in anurans. These hypobranchial placodes were recognized as ectodermal thickenings situated ventral to the second and third pharyngeal pouch that give rise to neurons of unknown fate. Here, the development of hypobranchial placodes in Xenopus laevis is described in more detail using in situ hybridization and immunohistochemistry for various placodal ( Six1, Eya1) and neurogenic ( NGNR-1, NeuroD, Delta-1, Hu, acetylated tubulin) markers. Moreover, the fate of hypobranchial placodes was determined by analyzing tadpoles that had received orthotopic grafts of ventral branchial arch ectoderm at embryonic stages from donor embryos injected with the lineage tracer green fluorescent protein. The neurogenic epibranchial and hypobranchial placodes are shown to develop in certain subregions of a broader branchial placodal area as defined by Six1 and Eya1 expression, viz., adjacent to the dorsal and ventral tip of the pharyngeal pouches, respectively. Grafting experiments show that each of the two hypobranchial placodes gives rise to a small and previously undescribed hypobranchial ganglion (identified by its immunoreactivity for the neuron-specific Hu protein) of unknown function located in the ventral branchial arch region. No contributions of hypobranchial placodes to any other ganglia (including cardiac ganglia and the ganglia of branchiomeric nerves located dorsal to pharyngeal pouches) were found.     

Teeth before jaws? Comparative analysis of the structure and development of the external and internal scales in the extinct jawless vertebrate Loganellia scotica

Traditional hypotheses posit that teeth evolved from dermal scales, through the expansion of odontogenetically competent ectoderm into the mouth of jawless vertebrates. The discovery of tooth‐like scales inside thelodonts, an extinct group of jawless vertebrates, led to the alternative hypothesis that teeth evolved from endodermal derivatives and that there exists a fundamental developmental and phylogenetic distinction between oral/pharyngeal and external odontodes. We set out a test of this latter hypothesis, examining the development of scales of the thelodont Loganellia scotica using synchrotron radiation X‐ray tomographic microscopy (SRXTM). We reveal that the internal scales are organized into fused patches and rows, a key distinction from the discrete dermal scales. The pattern of growth of oral scale patches is polarized, but not along a particular vector, whereas pharyngeal scale rows grew along a vector. Our test of the phylogenetic distribution of oral and pharyngeal scales and teeth in vertebrates indicates that odontodes are first expressed in an external position. Internal scales, where present, are always located near to external orifices; the sequential development of pharyngeal scales in Loganellia is peculiar among thelodonts and other stem gnathostomes. It represents a convergence on, rather than the establishment of, the developmental pattern underpinning tooth replacement in jawed vertebrates. The available evidence suggests that internal odontodes evolved through the expansion of odontogenic competence from external to internal epithelia.     

An Ancient Gene Network Is Co-opted for Teeth on Old and New Jaws

Vertebrate dentitions originated in the posterior pharynx of jawless fishes more than half a billion years ago. As gnathostomes (jawed vertebrates) evolved, teeth developed on oral jaws and helped to establish the dominance of this lineage on land and in the sea. The advent of oral jaws was facilitated, in part, by absence of hox gene expression in the first, most anterior, pharyngeal arch. Much later in evolutionary time, teleost fishes evolved a novel toothed jaw in the pharynx, the location of the first vertebrate teeth. To examine the evolutionary modularity of dentitions, we asked whether oral and pharyngeal teeth develop using common or independent gene regulatory pathways. First, we showed that tooth number is correlated on oral and pharyngeal jaws across species of cichlid fishes from Lake Malawi (East Africa), suggestive of common regulatory mechanisms for tooth initiation. Surprisingly, we found that cichlid pharyngeal dentitions develop in a region of dense hox gene expression. Thus, regulation of tooth number is conserved, despite distinct developmental environments of oral and pharyngeal jaws; pharyngeal jaws occupy hox-positive, endodermal sites, and oral jaws develop in hox-negative regions with ectodermal cell contributions. Next, we studied the expression of a dental gene network for tooth initiation, most genes of which are similarly deployed across the two disparate jaw sites. This collection of genes includes members of the ectodysplasin pathway, eda and edar, expressed identically during the patterning of oral and pharyngeal teeth. Taken together, these data suggest that pharyngeal teeth of jawless vertebrates utilized an ancient gene network before the origin of oral jaws, oral teeth, and ectodermal appendages. The first vertebrate dentition likely appeared in a hox-positive, endodermal environment and expressed a genetic program including ectodysplasin pathway genes. This ancient regulatory circuit was co-opted and modified for teeth in oral jaws of the first jawed vertebrate, and subsequently deployed as jaws enveloped teeth on novel pharyngeal jaws. Our data highlight an amazing modularity of jaws and teeth as they coevolved during the history of vertebrates. We exploit this diversity to infer a core dental gene network, common to the first tooth and all of its descendants.     

Early development and replacement of the stickleback dentition

Teeth have long served as a model system to study basic questions about vertebrate organogenesis, morphogenesis, and evolution. In nonmammalian vertebrates, teeth typically regenerate throughout adult life. Fish have evolved a tremendous diversity in dental patterning in both their oral and pharyngeal dentitions, offering numerous opportunities to study how morphology develops, regenerates, and evolves in different lineages. Threespine stickleback fish (Gasterosteus aculeatus) have emerged as a new system to study how morphology evolves, and provide a particularly powerful system to study the development and evolution of dental morphology. Here, we describe the oral and pharyngeal dentitions of stickleback fish, providing additional morphological, histological, and molecular evidence for homology of oral and pharyngeal teeth. Focusing on the ventral pharyngeal dentition in a dense developmental time course of lab‐reared fish, we describe the temporal and spatial consensus sequence of early tooth formation. Early in development, this sequence is highly stereotypical and consists of seventeen primary teeth forming the early tooth field, followed by the first tooth replacement event. Comparing this detailed morphological and ontogenetic sequence to that described in other fish reveals that major changes to how dental morphology arises and regenerates have evolved across different fish lineages. J. Morphol. 277:1072–1083, 2016. © 2016 Wiley Periodicals, Inc.     

Ultrastructural features of the tegumental surface of a new metacercaria, Nematostrigea sp. (Trematoda: Strigeidae), with a search for potential taxonomically informative characters

The tegumental surface of a new strigeid metacercaria, Nematostrigea sp., which is a parasite of the freshwater fish Channa gachua (Hamilton) in central Vietnam, is described for the first time using scanning (SEM) and transmission (TEM) electron microscopy. In addition to the general tegumental surface in various parts of the body, details of the surface of the suckers, lappets and holdfast organ are presented, as are variations in the form and distribution of the body spines. As good taxonomic criteria are few in diplostomoid metacercariae at both specific and generic levels, a number of the ultrastructural features revealed may prove to represent taxonomically informative characters. These include the presence of: two rings of dome-shaped papillae localised at different levels on the rim of the oral sucker, a single ring of ciliated papillae on the inner margin of the ventral sucker and a band of dome-shaped papillae along the lateral margins of the broad body-fold in the ventral forebody; an unarmed oral sucker and anteroventral surface of the forebody, although the latter bears protuberant secretory pores; an armed ventral sucker covered by six-pointed spines, except on its rim; multi-pointed spines along the dorsal and ventral sides of the forebody, with the number of their teeth increasing posteriorly; multi-pointed spines on the forebody which gradually transform into single-pointed, more widely distributed spines on the hindbody, disappearing completely at posterior end of the body; the surface of the lappets with a particular distribution of pores leading to three types of secretory glands and three topographical modifications (areas where the surface is smooth, bears digitiform processes or bears recurved, dagger-shaped spines); and the surface of the holdfast organ which is covered with densely packed, straight or slightly curved, simple spines on its lateral surface but is smooth medially.     

The nervous system of the tube-worm Chaetopterus variopedatus (Polychaeta)

Silver impregnation of serial histological sections of the tubeworm Chaetopterus variopedatus revealed the presence of a subepidermal nervous system. The anterior nervous system is delimited by the first 11 segments and comprises (1) two dorsolateral cerebral ganglia and lateral instead of ventral nerve cords which are widely separated and thus connected by unusually long commissures, (2) a pharyngeal ganglion in the fourth segment which is connected to the cerebral ganglia by pharyngeal nerves and constitutes along with the pharyngeal plexus a stomatogastric or enteric nervous system, and (3) small, presumably segmental ganglionic swellings along the lateral nerve cords from which emerge commissures and parapodial nerves. No subesophageal ganglion or periesophageal connective could be identified. The lateral nerve cords converge toward the midline in the 12th segment to form the posterior nervous system comprising a pair of ventromedian nerve cords with their repetitive segmental ganglia from which emerge numerous short commissures and three segmental nerves coursing toward the dorsal and ventral regions of parapods and toward the neuropod. Light and electron microscopic investigations of cerebral and segmental ganglia showed an arrangement of inner neuropile and of unipolar neuron somata at the periphery. The neuropile comprises numerous neurites ranging in diameter from 0.5 to 10 μm and making polarized or symmetrical synaptic junctions with each other. The pharyngeal ganglion consists of a similar neuropile and of a large mass of cell bodies which is traversed by an elaborate network of sinuses and harbors three types of neurosecretory cells in addition to the conventional neuron somata. These findings are interpreted in the framework of the highly specialized morphological features and habits of Chaetopterus, and the welldeveloped stomatogastric system is considered to be related to control of the feeding activities.     

The odontode explosion: The origin of tooth‐like structures in vertebrates

Essentially we show recent data to shed new light on the thorny controversy of how teeth arose in evolution. Essentially we show (a) how teeth can form equally from any epithelium, be it endoderm, ectoderm or a combination of the two and (b) that the gene expression programs of oral versus pharyngeal teeth are remarkably similar. Classic theories suggest that (i) skin denticles evolved first and odontode‐inductive surface ectoderm merged inside the oral cavity to form teeth (the ‘outside‐in’ hypothesis) or that (ii) patterned odontodes evolved first from endoderm deep inside the pharyngeal cavity (the ‘inside‐out’ hypothesis). We propose a new perspective that views odontodes as structures sharing a deep molecular homology, united by sets of co‐expressed genes defining a competent thickened epithelium and a collaborative neural crest‐derived ectomesenchyme. Simply put, odontodes develop ‘inside and out’, wherever and whenever these co‐expressed gene sets signal to one another. Our perspective complements the classic theories and highlights an agenda for specific experimental manipulations in model and non‐model organisms.     

Morphogenesis in Selaginella. III. Meristem determination and cell differentiation.

Selaginella willdenovii Baker is a prostrate vascular cryptogam with a dorsiventral stem. At each major branching of the stem tip a dorsal and a ventral angle meristem are formed. The ventral meristem becomes determined as a root and the dorsal meristem as a shoot. Indoleacetic acid (IAA) is transported basipetally in the stem and has been found to be the regulatory agent for meristem determination both in vitro and in vivo.Growth measurements of intact plants indicated that the sequence of development for each stem unit is frond expansion, internodal elongation, ventral meristem growth as a root, and dorsal meristem growth as a shoot. The principal experimental findings of this study are as follows. Triiodobenzoic acid (TIBA), an inhibitor of auxin transport alters the normal pattern of development in intact plants, causing ventral meristems to develop as shoots and dorsal meristems to develop precociously. Dorsal meristems grown in sterile culture on an auxin-free medium develop as shoots, but in the presence of IAA develop as roots. Meristems transferred after excision from auxin-free to plus-auxin medium on successive days showed an increasing tendency to develop as shoots, with more than 50% doing so by day 5. The mitotic index is low at the time of excision of the meristem, rises to a peak on day 5 and then declines.     

Glyoxylic acid induced fluorescence in the nervous system of Gyratrix hermaphroditus (Kalyptorhynchia,Polycystididae)

Catecholamines (CAs) are found in the neuropile of the brain, in 3 pairs of longitudinal nerve cords, in the transverse ventral commissure, in anterior ventral and dorsal nerves, in two pharyngeal nerve rings and in 24 neurons in the nervous system of Gyratrix hermaphroditus. The CA distribution pattern in compared with those of other neuroactive substances. Homology of neurons in the family of Polycystididae and in Plathelminthes in general is discussed.     

Sound production in the cichlid Tilapia mossambica Peters

Aquarium-bred adult and juvenile Tilapia mossambica Peters can produce sounds ofvarying frequency, duration and intensity. However, minor environmental disturbancesmay cause the fish to fall silent for long periods. The sounds produced by excited feedingfishes are different from those produced by territorial males and from those emitted by fryswimming in school formation. The frequency of the sounds recorded varied from about1–16 kHz; no data are available on frequencies lower than 1 kHz. The sound producingmechanism consists of a single ventral and two dorsal pharyngeals located in the buccalcavity and provided with numerous small teeth. These teeth have a specially modifieddistal surface area which is already evident in younger fish. Young Tilapia , including3-week old fry, are able to emit sounds as soon as a sufficient number of teeth havedeveloped in the pharyngeal region.     

Further structures in the jaw apparatus of Limnognathia maerski (Micrognathozoa), with notes on the phylogeny of the Gnathifera

The jaws of Limnognathia maerski, Micrognathozoa, were investigated with light- and scanning electron microscopy. The study yielded several new structures and sclerites, including the ventral part of main jaw, the pharyngeal lamellae, the manus, the dorsal and ventral fibularium teeth, and a reinterpretation of the fibularium compartmentalization. Furthermore, it was shown that several jaw elements are composed of densely packed rods. Comparison with Rotifera and Gnathostomulida suggested that the micrognathozoan main jaw is homologous with the rotifer incus and the gnathostomulid articularium and that the pseudophalangids (the ventral jaws) and their associated sclerites correspond to the rotifer mallei. These results imply that Micrognathozoa is more closely related to Rotifera than to Gnathostomulida.     

Low divergence in Dlx gene expression between dentitions of the medaka (Oryzias latipes) versus high level of expression shuffling in osteichtyans

SUMMARY Serially homologous structures are believed to originate from the redeployment of a genetic cascade in different locations of the body. Serial homologs may diverge at the genetic and morphological level and acquire developmental independency (individualization). Teeth are repeated units that form dentitions found on different bones of the oral–pharyngeal cavity in gnathostomes and provide a good model to study such processes. Previous comparisons of dlx gene expression patterns between mouse oral teeth and zebrafish pharyngeal teeth showed a high level of divergence. Furthermore, these genes are differentially expressed in different teeth of the zebrafish, and in the mouse they are responsible for tooth identity (incisors vs. molars). We examined the potential divergence of dlx gene expression between oral and pharyngeal teeth by examining the expression pattern in the development of the first generation teeth of the medaka and comparing it with data from the zebrafish and the mouse. Out of the seven medaka dlx genes, five are expressed during odontogenesis compared with six in both the zebrafish and the mouse. The only difference observed between oral and pharyngeal teeth in the medaka is an earlier expression of dlx5a in the oral dental epithelium. The subset of dlx genes expressed in the medaka, zebrafish, and mouse is slightly different but their detailed expression patterns are highly divergent. Our results demonstrate a low constraint on dlx gene expression shuffling in the odontogenic cascade within osteichtyans but the non-individualization of oral and pharyngeal dentitions in the medaka.     

3D morphology of pharyngeal dentition of the genus Capoeta (Cyprinidae): Implications for taxonomy and phylogeny

Capoeta is a herbivorous cyprinid fish genus, widely distributed in water bodies of Western Asia. Recent species show a distinct biogeographic pattern with endemic distribution in large fluvial drainage basins. As other cyprinids, the species of this genus are characterized by the presence of the pharyngeal bone with pharyngeal teeth. Despite this, the detailed morphology of the pharyngeal teeth, its interspecific and topologic variations, and the importance for taxonomy and phylogeny of the genus Capoeta are still not established. For the first time, a detailed comprehensive study of the pharyngeal dentition of 10 Capoeta species has been provided. The morphologic study of the pharyngeal dentition bases on the 3D microtomography and follows the purpose to evaluate the potential taxonomic and phylogenetic signals of these elements, as well as to study interspecific and topologic variations of the pharyngeal teeth. In this study, we propose a new methodology to categorize the studied pharyngeal teeth in 18 shape classes. The results of this study show that the detailed 3D morphology of the pharyngeal teeth is a useful tool for the identification of isolated teeth at the generic and/or specific level and that in certain cases, the tooth position in the teeth rows can be identified. Additionally, the preliminary analysis shows that the morphology of the pharyngeal teeth provides a potential phylogenetic signal. Both these patterns are very important for the taxonomy of cyprinid fishes and especially can be applied to fossil records.     

Autoradiographic observations on developing and growing claws of reptiles

Alibardi, L. 2010. Autoradiographic observations on developing and growing claws of reptiles. —Acta Zoologica (Stockholm) 91 : 233–241 The present qualitative autoradiographic analysis aims to present the main features of morphogenesis and growth of claws in reptiles. Lizard embryos treated with tritiated thymidine reveal that epidermal cell proliferation in terminal digits is prevalent in the dorsal side and gives origin to the curved unguis of the claw. Less proliferation occurs in the ventral side of the digit tip where the concave sub‐unguis is derived. Adult claws of a turtle show that thymidine‐labelled cells are present along most of the epidermis of the claw, especially at the claw tip. Also, injection of tritiated histidine and proline, indicating active protein synthesis, confirm autoradiographic labelling along most of the epidermis of claws, in particular at the apical tip. The present study indicates that proximal matrix regions, as have been described in mammalian nails, are absent in reptiles. This pattern of claw growth probably derives from that of terminal digital scales. In fact reptilian (and avian) claws are formed from a modification of scales, a different condition from that present in mammals.     

The biology of the Pe-ret' Toad, Otophryne robusta- (Microhylidae), with special consideration of its fossorial larva and systematic relationships

Adult and larval Otophryne robusta- were collected in Colombia, South America. Although this genus has been assigned to the family Microhylidae, a variety of both adult and larval features distinguish it from all other microhylids. The adult is a diurnally active leaf mimic with complex agonistic behaviours and vocalizations. It tends to walk rather than hop, and does not burrow in captivity. The larva is unique in having minute, dagger-like, keratinized teeth and a sinistral spiracle at the tip of a long tube. The mature larva lives shallowly buried in sand at the bottom of clear, shallow streams. The anatomy of the tadpole was examined for clues to how it burrows into and survives in sand, as well as to the correct phylogenetic association of the genus. Internally, the tadpole is most similar to microhylid tadpoles and has a wealth of oral features (e.g. unperforated internal nares, branchial food traps arranged in crescentic organs, ventral velum divided on the midline, glottis located rostral to the free edge of the ventral velum, large gill filters etc.) that characterize that family. Most, if not all, of the unique features of the Otophryne larva can be associated with its fossorial existence. The arrangement of the muscles suggest that it can actively raise and lower its snout during burrowing and possibly dorsiflex its head on its vertebral column. Although the larval teeth first suggest carnivory, many features indicate that maerophagy is not possible. Stomach contents include a variety of bacteria and micro-organisms, but no fragments of macroscopic animals. We conclude that the Otophryne tadpole is a microphagous suspension feeder and its teeth are more important for keeping sand grains out of its mouth than for grasping prey. Since the O. robusta larva does not burrow deeply, the tip of its spiracular tube probably extends upward above the sandy bottom and into the current. In this position pressure would be lower at the spiracle than at the mouth and a current could be passively drawn (by the Bernoulli effect) through the oral cavity for feeding and respiration. If this is correct then the Otophryne larva is the first fossorial vertebrate known to passively filter-feed. All features of the tadpole, except the keratinized teeth and sinistral spiracle, indicate an affinity of Otophryne-/i with South American microhylids. The tadpole and adult are, however, so unusual as to warrant subfamilial status+ADs- we propose the subfamily Otophryninac for this monotypic genus.     

Growth and morphological development of larval and juvenileepinephelus bruneus (perciformes: Serranidae)

The growth and morphological development of larval and juvenileEpinephelus bruneus were examined in a hatchery-reared series. Average body length (BL) of newly-hatched larvae was 1.99 mm, the larvae growing to an average of 3.96 mm by day 10, 6.97 mm by day 20, 12.8 mm by day 30, 22.1 mm by day 40 and 24.7 mm by day 45 after hatching. Newly-hatched larvae had many mucous cells in the entire body epidermis. By about 4 mm BL, the larvae had developed pigment patterns peculiar to epinepheline fishes, including melanophores on the dorsal part of the gut, on the tips of the second dorsal and pelvic fin spines, and in a cluster on the ventral surface of the tail. Spinelets on the second dorsal and pelvic fin spines, the preopercular angle spine and the supraocular spine, had started to develop by about 6 mm BL. The notochord tip was in the process of flexion in larvae of 6–8 mm BL, by which time major spines, pigments and jaw teeth had started to appear. Fin ray counts had attained the adult complement at 10 mm BL. After larvae reached 17 mm BL, elements of juvenile coloration in the form of more or less densely-pigmented patches started to appear on the body. Squamation started at 20 mm BL. Major head spines had disappeared or became relatively smaller and lost their serrations by 20–25 mm BL.     

Pelagic eggs and larvae of Coelorinchus kishinouyei (Gadiformes: Macrouridae) collected from Suruga Bay, Japan

Pelagic eggs and larvae of the macrourid fish Coelorinchus kishinouyei, collected from Suruga Bay, southern Japan and subsequently identified by 16S rRNA gene nucleotide sequences, are described. The spherical eggs, 1.18–1.31 mm in diameter, contained a single oil globule, 0.28–0.33 mm in diameter, and had hexagonally patterned ornamentation on the chorion, 0.017–0.022 mm in width. Melanophores were present on the embryo, yolk and oil globule after the blastopore had closed. Within 1 day after hatching, the body axis of the yolk-sac larvae was bent slightly at the anterior trunk region. During this stage many melanophores formed on the head, trunk, tail, yolk and oil globule, along with small irregular wrinkles on the dorsal and ventral finfolds. Pelagic eggs (after the caudal end of the embryo had detached from the yolk) and yolk-sac larvae also developed xanthophores on the embryo and yolk, and head, trunk, dorsal and ventral finfolds just before tail tip, and yolk, respectively. The pelagic larvae had a short tail, stalked pectoral-fin base and no elongate first dorsal and pelvic-fin rays. Three clusters of melanophores were present on the tail (anterior two embedded to muscle and one just before tail tip subsequently lost with development) and a cluster around the anus (beyond 3.9 mm head length). Nucleotide sequence analyses of comparative adult specimens appeared to confirm a previous proposal that C. productus is a junior synonym of C. anatirostris.