Development of dermal denticles in skates (Chondrichthyes, Batoidea): Patterning and cellular differentiation

Miyake, Tsutomu; Vaglia, Janet L.; Taylor, Lawrence H.; Hall, Brian K.

doi:10.1002/(sici)1097-4687(199907)241:1<61::aid-jmor4>3.0.co;2-s

Cited by 43 publications

(36 citation statements)

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“…The histological data we obtained for embryonic oral tooth and caudal primary scale development in the dogfish are in accordance with those obtained previously in other elasmobranch species or at later stages of dogfish development [20,21]. In addition, our morphological and histological observations show that teeth and scales share morphogenetic similarities through four developmental stages, which are also shared with mammalian oral teeth and teleost pharyngeal or oral teeth [12,17,30].…”

Section: Discussionsupporting

confidence: 90%

“…In this species, histological observations support that tooth and dermal denticle development display similarities with that of osteichthyans [20,21]. Among the different subsets of dermal denticle described during dogfish embryogenesis by Mellinger and Wrisez [22], we chose to work on the earliest developing ones, the caudal primary scales.…”

Section: Introductionmentioning

confidence: 99%

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The homology of odontodes in gnathostomes: insights from Dlx gene expression in the dogfish, Scyliorhinus canicula

et al. 2011

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BackgroundTeeth and tooth-like structures, together named odontodes, are repeated organs thought to share a common evolutionary origin. These structures can be found in gnathostomes at different locations along the body: oral teeth in the jaws, teeth and denticles in the oral-pharyngeal cavity, and dermal denticles on elasmobranch skin. We, and other colleagues, had previously shown that teeth in any location were serially homologous because: i) pharyngeal and oral teeth develop through a common developmental module; and ii) the expression patterns of the Dlx genes during odontogenesis were highly divergent between species but almost identical between oral and pharyngeal dentitions within the same species. Here we examine Dlx gene expression in oral teeth and dermal denticles in order to test the hypothesis of serial homology between these odontodes.ResultsWe present a detailed comparison of the first developing teeth and dermal denticles (caudal primary scales) of the dogfish (Scyliorhinus canicula) and show that both odontodes develop through identical stages that correspond to the common stages of oral and pharyngeal odontogenesis. We identified six Dlx paralogs in the dogfish and found that three showed strong transcription in teeth and dermal denticles (Dlx3, Dlx4 and Dlx5) whereas a weak expression was detected for Dlx1 in dermal denticles and teeth, and for Dlx2 in dermal denticles. Very few differences in Dlx expression patterns could be detected between tooth and dermal denticle development, except for the absence of Dlx2 expression in teeth.ConclusionsTaken together, our histological and expression data strongly suggest that teeth and dermal denticles develop from the same developmental module and under the control of the same set of Dlx genes. Teeth and dermal denticles should therefore be considered as serial homologs developing through the initiation of a common gene regulatory network (GRN) at several body locations. This mechanism of heterotopy supports the 'inside and out' model that has been recently proposed for odontode evolution.

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Section: Discussionsupporting

confidence: 90%

Section: Introductionmentioning

confidence: 99%

The homology of odontodes in gnathostomes: insights from Dlx gene expression in the dogfish, Scyliorhinus canicula

et al. 2011

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“…Among gnathostomes (jawed vertebrates), the structural organization of the integumentary skeleton continues to vary taxonomically: the skull and integumentary elements of placoderms (Silurian to late Devonian, ~435-360 Ma) are characterized by cellular bone covered by a cellular dentine with polarized cell processes (semidentine), whereas the scalation of chondrichthyans [= odontodes (placoid scales)] consists of a superficial layer of enameloid, capping an orthodentine crown, attached to the dermis by bone of attachment (Goodrich, 1907;Miyake et al 1999; Ørvig, 1957;Jarvik, 1980;Dias & Richter, 2002 Anura osteoderm mostly dorsal body surface; usually multiple small polygonal elements creating a juxtaposed mosaic but sometimes larger plates fused to neural spines cellular bone (parallel-fibred and/or lamellar bone) non-stratified compact bone uncertain: hypothesized to include bone metaplasia Ruibal & Shoemaker, 1984 lamina calcarea distributed across body as a thin intradermal layer; sometimes segmented to form granular bodies known as dermolita acellular, non-collagenous matrix that contains proteoglycans (including glycosaminoglycans) and hydroxyapatite-like crystals homogeneous tissue uncertain: hypothesized to be deposited by fibroblasts Muzzi, 1968;Elkan, 1976;Sampson et al 1987;Toledo & Jared, 1993;Katchburian et al 2001;Schwinger et al 2001 Schmidt, 1914;Moss, 1969;Scheyer & Sander, 2004;Main et al 2005;Vickaryous & Hall, 2008 Lepidosauria osteoderm variable distribution: often restricted to head and/or dorsal body surface but may encase the entire body; highly polymorphic: granular, bead-like, vermiform, compound and imbricating scalelike shapes cellular bone (woven-fibred, parallelfibred, lamellar); calcified and unmineralized fibrous connective tissue; and (in some taxa) an enigmatic collagen-poor capping tissue often stratified into two distinct layers of which the basal portion is always bone (parallel-fibred or lamellar); superficial layer is variable and may consist of woven-fibred bone or an enigmatic collagenpoor tissue uncertain: evidence suggests both bone metaplasia and intramembranous ossification Moss, 1969;Zylberberg & Castanet, 1985;Levrat-Calviac et al 1986;Levrat-Calviac & Zylberberg, 1986 Testudines carapace skeletal complex consisting of multiple tightly articulating and fused bony elements enclosing the dorsal body surface (trunk), including the pectoral apparatus cellular bone (lamellar); plywood-like arrangement of collagen fibres in the external cortex of some trionychids trilaminar org...…”

Section: Early Evolution Of the Vertebrate Integumentary Skeletonmentioning

confidence: 99%

The integumentary skeleton of tetrapods: origin, evolution, and development

2009

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Although often overlooked, the integument of many tetrapods is reinforced by a morphologically and structurally diverse assemblage of skeletal elements. These elements are widely understood to be derivatives of the once all-encompassing dermal skeleton of stem-gnathostomes but most details of their evolution and development remain confused and uncertain. Herein we re-evaluate the tetrapod integumentary skeleton by integrating comparative developmental and tissue structure data. Three types of tetrapod integumentary elements are recognized: (1) osteoderms, common to representatives of most major taxonomic lineages; (2) dermal scales, unique to gymnophionans; and (3) the lamina calcarea, an enigmatic tissue found only in some anurans. As presently understood, all are derivatives of the ancestral cosmoid scale and all originate from scleroblastic neural crest cells. Osteoderms are plesiomorphic for tetrapods but demonstrate considerable lineage-specific variability in size, shape, and tissue structure and composition. While metaplastic ossification often plays a role in osteoderm development, it is not the exclusive mode of skeletogenesis. All osteoderms share a common origin within the dermis (at or adjacent to the stratum superficiale) and are composed primarily (but not exclusively) of osseous tissue. These data support the notion that all osteoderms are derivatives of a neural crest-derived osteogenic cell population (with possible matrix contributions from the overlying epidermis) and share a deep homology associated with the skeletogenic competence of the dermis. Gymnophionan dermal scales are structurally similar to the elasmoid scales of most teleosts and are not comparable with osteoderms. Whereas details of development are lacking, it is hypothesized that dermal scales are derivatives of an odontogenic neural crest cell population and that skeletogenesis is comparable with the formation of elasmoid scales. Little is known about the lamina calcarea. It is proposed that this tissue layer is also odontogenic in origin, but clearly further study is necessary. Although not homologous as organs, all elements of the integumentary skeleton share a basic and essential relationship with the integument, connecting them with the ancestral rhombic scale.

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“…A well-delimited dermal papilla during early morphogenesis of : ( A) an odontode in a chondrichthyan, the skate Leucoraja erinacea ( afterMiyake et al, 1999) ; ( B, C ) teeth on the mandible in the cichlid Hemichromis bimaculatus ; ( D, E) a denticle in the callichthyid Corydoras aeneus ; ( F, G ) an elasmoid scale in a cyprinid, the zebrafish Danio rerio. The arrows point to the epidermaldermal boundary.…”

mentioning

confidence: 99%

Formation of dermal skeletal and dental tissues in fish: a comparative and evolutionary approach

2003

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Osteichthyan and chondrichthyan fish present an astonishing diversity of skeletal and dental tissues that are often difficult to classify into the standard textbook categories of bone, cartilage, dentine and enamel. To address the question of how the tissues of the dermal skeleton evolved from the ancestral situation and gave rise to the diversity actually encountered, we review previous data on the development of a number of dermal skeletal elements (odontodes, teeth and dermal denticles, cranial dermal bones, postcranial dermal plates and scutes, elasmoid and ganoid scales, and fin rays). A comparison of developmental stages at the tissue level usually allows us to identify skeletogenic cell populations as either odontogenic or osteogenic on the basis of the place of formation of their dermal papillae and of the way of deposition of their tissues. Our studies support the evolutionary affinities (1) between odontodes, teeth and denticles, (2) between the ganoid scales of polypterids and the elasmoid scales of teleosts, and (3) to a lesser degree between the different bony elements. There is now ample evidence to ascertain that the tissues of the elasmoid scale are derived from dental and not from bony tissues. This review demonstrates the advantage that can be taken from developmental studies, at the tissue level, to infer evolutionary relationships within the dermal skeleton in chondrichthyans and osteichthyans.

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Development of dermal denticles in skates (Chondrichthyes, Batoidea): Patterning and cellular differentiation

Cited by 43 publications

References 83 publications

The homology of odontodes in gnathostomes: insights from Dlx gene expression in the dogfish, Scyliorhinus canicula

The homology of odontodes in gnathostomes: insights from Dlx gene expression in the dogfish, Scyliorhinus canicula

The integumentary skeleton of tetrapods: origin, evolution, and development

Formation of dermal skeletal and dental tissues in fish: a comparative and evolutionary approach

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