The anatomical placode in reptile scale morphogenesis indicates shared ancestry among skin appendages in amniotes

Di‐Poï, Nicolas; Milinkovitch, Michel C.

doi:10.1126/sciadv.1600708

Cited by 131 publications

(143 citation statements)

References 55 publications

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“…However, recent evidence has suggested that integumentary epithelial appendages are historically homologous, at least throughout all amniotes on the basis of the anatomical placode with conserved expression and function of GRN members [4]. Our results suggest this historical homology extends even further into vertebrate phylogeny and may encompass the integumentary epithelial appendages of all extant jawed vertebrates.…”

Section: Discussionmentioning

confidence: 50%

Developing an ancient epithelial appendage: FGF signalling regulates early tail denticle formation in sharks

Cooper

Martin

Rasch

et al. 2017

EvoDevo

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BackgroundVertebrate epithelial appendages constitute a diverse group of organs that includes integumentary structures such as reptilian scales, avian feathers and mammalian hair. Recent studies have provided new evidence for the homology of integumentary organ development throughout amniotes, despite their disparate final morphologies. These structures develop from conserved molecular signalling centres, known as epithelial placodes. It is not yet certain whether this homology extends beyond the integumentary organs of amniotes, as there is a lack of knowledge regarding their development in basal vertebrates. As the ancient sister lineage of bony vertebrates, extant chondrichthyans are well suited to testing the phylogenetic depth of this homology. Elasmobranchs (sharks, skates and rays) possess hard, mineralised epithelial appendages called odontodes, which include teeth and dermal denticles (placoid scales). Odontodes constitute some of the oldest known vertebrate integumentary appendages, predating the origin of gnathostomes. Here, we used an emerging model shark (Scyliorhinus canicula) to test the hypothesis that denticles are homologous to other placode-derived amniote integumentary organs. To examine the conservation of putative gene regulatory network (GRN) member function, we undertook small molecule inhibition of fibroblast growth factor (FGF) signalling during caudal denticle formation.ResultsWe show that during early caudal denticle morphogenesis, the shark expresses homologues of conserved developmental gene families, known to comprise a core GRN for early placode morphogenesis in amniotes. This includes conserved expression of FGFs, sonic hedgehog (shh) and bone morphogenetic protein 4 (bmp4). Additionally, we reveal that denticle placodes possess columnar epithelial cells with a reduced rate of proliferation, a conserved characteristic of amniote skin appendage development. Small molecule inhibition of FGF signalling revealed placode development is FGF dependent, and inhibiting FGF activity resulted in downregulation of shh and bmp4 expression, consistent with the expectation from comparison to the amniote integumentary appendage GRN.ConclusionOverall, these findings suggest the core GRN for building vertebrate integumentary epithelial appendages has been highly conserved over 450 million years. This provides evidence for the continuous, historical homology of epithelial appendage placodes throughout jawed vertebrates, from sharks to mammals. Epithelial placodes constitute the shared foundation upon which diverse vertebrate integumentary organs have evolved.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-017-0071-0) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 50%

Developing an ancient epithelial appendage: FGF signalling regulates early tail denticle formation in sharks

Cooper

Martin

Rasch

et al. 2017

EvoDevo

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“…Recently, we have shown that scaffoldin of the chicken is expressed in the embryonic periderm and in epithelial cells that support the morphogenesis of claws and feathers by providing a transient epithelial scaffold which degenerates after maturation of these skin appendages31. These data contributed to the evolutionary-developmental model that connects the embryonic archosaur scale and feathers16171853. The identification of the genes encoding scaffoldins 1 and 2 will facilitate the determination of their expression during embryonic development and during the shedding cycle of snakes in future studies.…”

Section: Discussionmentioning

confidence: 93%

“…Signaling between the epidermis and the underlying dermis controls the patterning of the epidermis and the formation of skin appendages15161718. While differentiation of keratinocytes in the mammalian epidermis involves continuous alterations of cell structures and movement of cells towards the body surface, keratinocyte differentiation in squamates results in the formation of distinct non-interconvertible layers that remain stable for several weeks before they are shed together89.…”

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confidence: 99%

Identification and comparative analysis of the epidermal differentiation complex in snakes

Holthaus

Mlitz

Strasser

et al. 2017

Sci Rep

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The epidermis of snakes efficiently protects against dehydration and mechanical stress. However, only few proteins of the epidermal barrier to the environment have so far been identified in snakes. Here, we determined the organization of the Epidermal Differentiation Complex (EDC), a cluster of genes encoding protein constituents of cornified epidermal structures, in snakes and compared it to the EDCs of other squamates and non-squamate reptiles. The EDC of snakes displays shared synteny with that of the green anole lizard, including the presence of a cluster of corneous beta-protein (CBP)/beta-keratin genes. We found that a unique CBP comprising 4 putative beta-sheets and multiple cysteine-rich EDC proteins are conserved in all snakes and other squamates investigated. Comparative genomics of squamates suggests that the evolution of snakes was associated with a gene duplication generating two isoforms of the S100 fused-type protein, scaffoldin, the origin of distinct snake-specific EDC genes, and the loss of other genes that were present in the EDC of the last common ancestor of snakes and lizards. Taken together, our results provide new insights into the evolution of the skin in squamates and a basis for the characterization of the molecular composition of the epidermis in snakes.

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“…In zebrafish and in bearded lizard, mutations in the EDA/EDAR pathway lead to the absence of scales and teeth (Fig. b, c) . In chick scaleless mutant, the absence of ESC and F is due to a FGF20 deletion (Fig.…”

Section: Conservation Of Placode Regulating Pathwaysmentioning

confidence: 97%

Getting to the root of scales, feather and hair: As deep as odontodes?

Dhouailly

Godefroit

Martin

et al. 2017

Experimental Dermatology

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While every jawed vertebrate, or its recent ancestor, possesses teeth, skin appendages are characteristic of the living clades: skin denticles (odontodes) in chondrichthyans, dermal scales in teleosts, ducted multicellular glands in amphibians, epidermal scales in squamates, feathers in birds and hair‐gland complexes in mammals, all of them showing a dense periodic patterning. While the odontode origin of teleost scales is generally accepted, the origin of both feather and hair is still debated. They appear long before mammals and birds, at least in the Jurassic in mammaliaforms and in ornithodires (pterosaurs and dinosaurs), and are contemporary to scales of early squamates. Epidermal scales might have appeared several times in evolution, and basal amniotes could not have developed a scaled dry integument, as the function of hair follicle requires its association with glands. In areas such as amnion, cornea or plantar pads, the formation of feather and hair is prevented early in embryogenesis, but can be easily reverted by playing with the Wnt/BMP/Shh pathways, which both imply the plasticity and the default competence of ectoderm. Conserved ectodermal/mesenchymal signalling pathways lead to placode formation, while later the crosstalk differs, as well as the final performing tissue(s): both epidermis and dermis for teeth and odontodes, mostly dermis for teleosts scales and only epidermis for squamate scale, feather and hair. We therefore suggest that tooth, dermal scale, epidermal scale, feather and hair evolved in parallel from a shared placode/dermal cell unit, which was present in a common ancestor, an early vertebrate gnathostome with odontodes, ca. 420 million years ago.

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The anatomical placode in reptile scale morphogenesis indicates shared ancestry among skin appendages in amniotes

Abstract: Researchers show that scales, feathers, and hairs of reptiles, birds, and mammals evolved from the scales of their common reptilian ancestor.

Cited by 131 publications

References 55 publications

Developing an ancient epithelial appendage: FGF signalling regulates early tail denticle formation in sharks

Developing an ancient epithelial appendage: FGF signalling regulates early tail denticle formation in sharks

Identification and comparative analysis of the epidermal differentiation complex in snakes

Getting to the root of scales, feather and hair: As deep as odontodes?

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