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

Published on Jun 1, 2016in Science Advances
· DOI :10.1126/sciadv.1600708
Nicolas Di-Poï9
Estimated H-index: 9
(University of Geneva),
Michel C. Milinkovitch38
Estimated H-index: 38
(Swiss Institute of Bioinformatics)
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Abstract
Most mammals, birds, and reptiles are readily recognized by their hairs, feathers, and scales, respectively. However, the lack of fossil intermediate forms between scales and hairs and substantial differences in their morphogenesis and protein composition have fueled the controversy pertaining to their potential common ancestry for decades. Central to this debate is the apparent lack of an “anatomical placode” (that is, a local epidermal thickening characteristic of feathers’ and hairs’ early morphogenesis) in reptile scale development. Hence, scenarios have been proposed for the independent development of the anatomical placode in birds and mammals and parallel co-option of similar signaling pathways for their morphogenesis. Using histological and molecular techniques on developmental series of crocodiles and snakes, as well as of unique wild-type and EDA (ectodysplasin A)–deficient scaleless mutant lizards, we show for the first time that reptiles, including crocodiles and squamates, develop all the characteristics of an anatomical placode: columnar cells with reduced proliferation rate, as well as canonical spatial expression of placode and underlying dermal molecular markers. These results reveal a new evolutionary scenario where hairs, feathers, and scales of extant species are homologous structures inherited, with modification, from their shared reptilian ancestor’s skin appendages already characterized by an anatomical placode and associated signaling molecules.
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  • References (50)
  • Citations (26)
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References50
Newest
Published on Jan 1, 2016in Acta Zoologica1.01
Lorenzo Alibardi27
Estimated H-index: 27
(UNIBO: University of Bologna),
Daniela Minelli4
Estimated H-index: 4
(UNIBO: University of Bologna)
Cell proliferation in forming shield scutes has been studied by immunofluorescence in embryos of turtle, alligator and snake after injection of 5-bromo-deoxy-uridine. Hinge regions of scutes in alligator and turtle carapace derive from an initial waving and invagination of the epidermis that contains 5-bromo-deoxy-uridine-labelled cells. This suggests that down growth of the epidermis into the dermis is driven by local proliferation in addition to dermal anchorage and stabilization of hinge regi...
Published on May 1, 2006in Cell Death & Differentiation8.09
G Courtois1
Estimated H-index: 1
(French Institute of Health and Medical Research),
A Smahi1
Estimated H-index: 1
The recent identification of genetic diseases (incontinentia pigmenti, anhidrotic ectodermal dysplasia with immunodeficiency and cylindromatosis) resulting from mutations affecting components of the nuclear factor-j B( NF-jB) signaling pathway provides a unique opportunity to understand the function of NF-jB in vivo. Besides confirming the importance of NF-jB in innate and acquired immunity or bone mass control, analysis of these diseases has uncovered new critical roles played by this transcrip...
Published on Jun 1, 2015in Genome Biology and Evolution3.73
Athanasia C. Tzika17
Estimated H-index: 17
(Swiss Institute of Bioinformatics),
Asier Ullate-Agote2
Estimated H-index: 2
(Swiss Institute of Bioinformatics)
+ 1 AuthorsMichel C. Milinkovitch38
Estimated H-index: 38
(Swiss Institute of Bioinformatics)
Despite the availability of deep-sequencing techniques, genomic and transcriptomic data remain unevenly distributed across phylogenetic groups. For example, reptiles are poorly represented in sequence databases, hindering functional evolutionary and developmental studies in these lineages substantially more diverse than mammals. In addition, different studies use different assembly and annotation protocols, inhibiting meaningful comparisons. Here, we present the “Reptilian Transcriptomes Databas...
Published on Jun 1, 2015in Evolution & Development1.82
Jacob M. Musser6
Estimated H-index: 6
(Yale University),
Günter P. Wagner61
Estimated H-index: 61
(Yale University),
Richard O. Prum46
Estimated H-index: 46
(AMNH: American Museum of Natural History)
SUMMARY Feathers are an evolutionary novelty found in all extant birds. Despite recent progress investigating feather development and a revolution in dinosaur paleontology, the relationship of feathers to other amniote skin appendages, particularly reptile scales, remains unclear. Disagreement arises primarily from the observation that feathers and avian scutate scales exhibit an anatomical placode—defined as an epidermal thickening—in early development, whereas alligator and other avian scales ...
Published on Jan 28, 2015in eLife7.55
Natasha M O'Brown2
Estimated H-index: 2
(Stanford University),
Brian R. Summers8
Estimated H-index: 8
(Stanford University)
+ 2 AuthorsDavid M. Kingsley55
Estimated H-index: 55
(Stanford University)
Armor plate changes in sticklebacks are a classic example of repeated adaptive evolution. Previous studies identified ectodysplasin (EDA) gene as the major locus controlling recurrent plate loss in freshwater fish, though the causative DNA alterations were not known. Here we show that freshwater EDA alleles have cis-acting regulatory changes that reduce expression in developing plates and spines. An identical T → G base pair change is found in EDA enhancers of divergent low-plated fish. Recreati...
Published on Aug 1, 2014in Development5.76
Jacqueline E. Moustakas-Verho4
Estimated H-index: 4
(UH: University of Helsinki),
Roland Zimm2
Estimated H-index: 2
(UH: University of Helsinki)
+ 7 AuthorsScott F. Gilbert40
Estimated H-index: 40
(Swarthmore College)
The origin of the turtle shell over 200 million years ago greatly modified the amniote body plan, and the morphological plasticity of the shell has promoted the adaptive radiation of turtles. The shell, comprising a dorsal carapace and a ventral plastron, is a layered structure formed by basal endochondral axial skeletal elements (ribs, vertebrae) and plates of bone, which are overlain by keratinous ectodermal scutes. Studies of turtle development have mostly focused on the bones of the shell; h...
Published on Mar 1, 2014in Developmental Cell9.19
Laura Ahtiainen13
Estimated H-index: 13
(UH: University of Helsinki),
Sylvie Lefebvre7
Estimated H-index: 7
(UH: University of Helsinki)
+ 5 AuthorsMarja L. Mikkola36
Estimated H-index: 36
(UH: University of Helsinki)
Summary Epithelial reorganization involves coordinated changes in cell shapes and movements. This restructuring occurs during formation of placodes, ectodermal thickenings that initiate the morphogenesis of epithelial organs including hair, mammary gland, and tooth. Signaling pathways in ectodermal placode formation are well known, but the cellular mechanisms have remained ill defined. We established imaging methodology for live visualization of embryonic skin explants during the first wave of h...
Published on Jan 1, 2014in Seminars in Cell & Developmental Biology5.46
Leah C. Biggs3
Estimated H-index: 3
(UH: University of Helsinki),
Marja L. Mikkola36
Estimated H-index: 36
(UH: University of Helsinki)
Abstract The embryonic surface ectoderm gives rise to the epidermis and ectodermal appendages including hair follicles, teeth, scales, feathers, and mammary, sweat, and salivary glands. Their early development proceeds largely the same through the induction, placode, and bud stages prior to diversification of epithelial morphogenesis which ultimately produces the wide array of mature organs. In this review we summarize the current knowledge on the molecular and cellular processes driving the sha...
Published on Feb 1, 2013in Cold Spring Harbor Perspectives in Biology9.11
Xinhong Lim10
Estimated H-index: 10
(Stanford University),
RoelNUSSE87
Estimated H-index: 87
(Stanford University)
The skin and its appendages constitute the largest organ of the body. Its stratified epithelia offer protection from environmental stresses such as dehydration, irradiation, mechanical trauma, and pathogenic infection, whereas its appendages, like hair and sebaceous glands, help regulate body temperature as well as influence animal interaction and social behavior through camouflage and sexual signaling. To respond to and function effectively in a dynamic external environment, the skin and its ap...
Published on Jan 4, 2013in Science41.04
Michel C. Milinkovitch38
Estimated H-index: 38
(University of Geneva),
Liana Manukyan3
Estimated H-index: 3
(University of Geneva)
+ 5 AuthorsMatthias Zwicker34
Estimated H-index: 34
(University of Bern)
Various lineages of amniotes display keratinized skin appendages (feathers, hairs, and scales) that differentiate in the embryo from genetically controlled developmental units whose spatial organization is patterned by reaction-diffusion mechanisms (RDMs). We show that, contrary to skin appendages in other amniotes (as well as body scales in crocodiles), face and jaws scales of crocodiles are random polygonal domains of highly keratinized skin, rather than genetically controlled elements, and em...
Cited By26
Newest
Published on 2019in Evodevo2.12
Rory L. Cooper3
Estimated H-index: 3
(University of Sheffield),
Victoria Lloyd (University of Sheffield)+ 3 AuthorsGareth J. Fraser17
Estimated H-index: 17
(UF: University of Florida)
Vertebrates possess a diverse range of integumentary epithelial appendages, including scales, feathers and hair. These structures share extensive early developmental homology, as they mostly originate from a conserved anatomical placode. In the context of avian epithelial appendages, feathers and scutate scales are known to develop from an anatomical placode. However, our understanding of avian reticulate (footpad) scale development remains unclear. Here, we demonstrate that reticulate scales de...
Published on Jun 1, 2019in Trends in Ecology and Evolution15.24
Michael J. Benton66
Estimated H-index: 66
(UoB: University of Bristol),
Danielle Dhouailly25
Estimated H-index: 25
+ 1 AuthorsMaria E. McNamara12
Estimated H-index: 12
(UCC: University College Cork)
Feathers have long been regarded as the innovation that drove the success of birds. However, feathers have been reported from close dinosaurian relatives of birds, and now from ornithischian dinosaurs and pterosaurs, the cousins of dinosaurs. Incomplete preservation makes these reports controversial. If true, these findings shift the origin of feathers back 80 million years before the origin of birds. Gene regulatory networks show the deep homology of scales, feathers, and hairs. Hair and feathe...
Published on Jul 1, 2019in iScience
Takanori Shono1
Estimated H-index: 1
(University of Sheffield),
Alexandre P. Thiery1
Estimated H-index: 1
(University of Sheffield)
+ 4 AuthorsGareth J. Fraser17
Estimated H-index: 17
(UF: University of Florida)
Summary Teleost fishes develop remarkable varieties of skin ornaments. The developmental basis of these structures is poorly understood. The order Tetraodontiformes includes diverse fishes such as the ocean sunfishes, triggerfishes, and pufferfishes, which exhibit a vast assortment of scale derivatives. Pufferfishes possess some of the most extreme scale derivatives, dermal spines, erected during their characteristic puffing behavior. We demonstrate that pufferfish scale-less spines develop thro...
Published on 2019in eLife7.55
Lotta Salomies (UH: University of Helsinki), Julia Eymann (UH: University of Helsinki)+ 1 AuthorsNicolas Di-Poï9
Estimated H-index: 9
(UH: University of Helsinki)
Published on Mar 4, 2019in The Journal of Comparative Neurology3.24
François Friocourt3
Estimated H-index: 3
(University of Paris),
Peter Kozulin7
Estimated H-index: 7
(UQ: University of Queensland)
+ 5 AuthorsAlain Chédotal58
Estimated H-index: 58
(University of Paris)
In Bilaterians, commissural neurons project their axons across the midline of the nervous system to target neurons on the opposite side. In mammals, midline crossing at the level of the hindbrain and spinal cord requires the Robo3 receptor which is transiently expressed by all commissural neurons. Unlike other Robo receptors, mammalian Robo3 receptors do not bind Slit ligands and promote midline crossing. Surprisingly, not much is known about Robo3 distribution and mechanism of action in other v...
Published on 2019in bioRxiv
Sergio Forcelloni1
Estimated H-index: 1
(Sapienza University of Rome),
Antonio Deiana2
Estimated H-index: 2
(Sapienza University of Rome),
Andrea Giansanti12
Estimated H-index: 12
(Sapienza University of Rome)
In a recent study, we have introduced an operational classification of the human proteome in three variants of disorder: ordered proteins (ORDPs), structured proteins with intrinsically disordered protein regions (IDPRs), intrinsically disordered proteins (IDPs). That classification was useful in functionally separating IDPRs from IDPs, which up until now have been generally considered as a whole. In this study, we corroborate this distinction by considering different physical-chemical and struc...
Published on Jun 26, 2019in Evolution3.57
Kathryn E. Stanchak1
Estimated H-index: 1
,
Jessica H. Arbour9
Estimated H-index: 9
,
Sharlene E. Santana15
Estimated H-index: 15
Published on May 1, 2019in Journal of Computational Physics2.85
Luis Miguel De Oliveira Vilaca1
Estimated H-index: 1
(Swiss Institute of Bioinformatics),
Michel C. Milinkovitch38
Estimated H-index: 38
(Swiss Institute of Bioinformatics),
Ricardo Ruiz-Baier15
Estimated H-index: 15
(University of Oxford)
Abstract We introduce a model for the mass transfer of molecular activators and inhibitors in two media separated by an interface, and study its interaction with the deformations exhibited by the two-layer skin tissue where they occur. The mathematical model results in a system of nonlinear advection-diffusion–reaction equations including cross-diffusion, and coupled with an interface elasticity problem. We propose a Galerkin method for the discretisation of the set of governing equations, invol...
Published on Apr 1, 2019in Experimental Dermatology2.87
Danielle Dhouailly25
Estimated H-index: 25
,
Pascal Godefroit20
Estimated H-index: 20
(Royal Belgian Institute of Natural Sciences)
+ 3 AuthorsOlav T. Oftedal12
Estimated H-index: 12
(SERC: Smithsonian Environmental Research Center)
While every jawed vertebrate, or its recent ancestor, possesses teeth, skin appendages are characteristic of the living clades: skin denticles (odontodes) in chondrichthyians, 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 debate...
Published on Feb 21, 2019in PLOS Biology
William Ho3
Estimated H-index: 3
(Edin.: University of Edinburgh),
Lucy Freem3
Estimated H-index: 3
(Edin.: University of Edinburgh)
+ 16 AuthorsPascal Schneider79
Estimated H-index: 79
(UNIL: University of Lausanne)
Feathers are arranged in a precise pattern in avian skin. They first arise during development in a row along the dorsal midline, with rows of new feather buds added sequentially in a spreading wave. We show that the patterning of feathers relies on coupled fibroblast growth factor (FGF) and bone morphogenetic protein (BMP) signalling together with mesenchymal cell movement, acting in a coordinated reaction-diffusion-taxis system. This periodic patterning system is partly mechanochemical, with me...
View next paperA new scenario for the evolutionary origin of hair, feather, and avian scales