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| Open AccessActuation enhances patterning in human neural tube organoids
Mechanical forces, along with gene regulatory networks and cell-cell signalling, play an important role in the complex organization of tissues. Here the authors describe devices that actively apply mechanical force to developing neural tube, demonstrating that mechanical forces increase growth and enhance patterning.
- Abdel Rahman Abdel Fattah
- , Brian Daza
- & Adrian Ranga
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Article
| Open AccessControl of mouse limb initiation and antero-posterior patterning by Meis transcription factors
Double conditional knockout of Meis1/2 in the limb forming region of mouse embryos results in the complete absence of limb, while embryos developed with one functional Meis allele, so identifying the role of Meis in antero-posterior and proximo-distal patterning.
- Irene Delgado
- , Giovanna Giovinazzo
- & Miguel Torres
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Article
| Open AccessCo-development of central and peripheral neurons with trunk mesendoderm in human elongating multi-lineage organized gastruloids
The authors generate EMLOs (elongating multi-lineage organized gastruloids): organoids that self-organize to form compartments with characteristics of the central nervous system, peripheral nervous system, mesenchyme, and gut tube.
- Zachary T. Olmsted
- & Janet L. Paluh
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Article
| Open AccessIn situ differentiation of iridophore crystallotypes underlies zebrafish stripe patterning
The skin of zebrafish is patterned by alternating blue stripes and yellow interstripes which arises from guanine crystal-containing cells called iridophores that reflect light. Here the authors track iridophores and see that they do not migrate between stripes and interstripes, but instead differentiate and proliferate in place based on their micro-environment.
- Dvir Gur
- , Emily J. Bain
- & David M. Parichy
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Article
| Open AccessInterpretation of morphogen gradients by a synthetic bistable circuit
Morphogen gradients can be dynamic and transient yet give rise to stable cellular patterns. Here the authors show that a synthetic morphogen-induced mutual inhibition circuit produces stable boundaries when the spatial average of morphogens falls within the region of bistability.
- Paul K. Grant
- , Gregory Szep
- & Andrew Phillips
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Article
| Open AccessMechanical forces drive ordered patterning of hair cells in the mammalian inner ear
The periodic organization of cells is typically associated with mechanisms based on intercellular signaling such as lateral inhibition and Turing patterning. Here the authors show that hair cells in the inner ear rearrange gradually into a checkerboard-like pattern through a tissue-wide shear motion that coordinates intercalation and delamination events.
- Roie Cohen
- , Liat Amir-Zilberstein
- & David Sprinzak
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Article
| Open AccessA theoretical model of Polycomb/Trithorax action unites stable epigenetic memory and dynamic regulation
Polycomb (PcG) and Trithorax (TrxG) group regulate several hundred target genes with important roles in development and disease. Here the authors combine experiment and theory to provide evidence that the Polycomb/Trithorax system has the potential for a rich repertoire of regulatory modes beyond simple epigenetic memory.
- Jeannette Reinig
- , Frank Ruge
- & Leonie Ringrose
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Article
| Open AccessStochastic pulsing of gene expression enables the generation of spatial patterns in Bacillus subtilis biofilms
Stochastic pulsing of gene expression can generate phenotypic diversity in a genetically identical population of cells. Here, the authors show that stochastic pulsing in the expression of a sigma factor enables the formation of spatial patterns in a multicellular system, Bacillus subtilis bacterial biofilms.
- Eugene Nadezhdin
- , Niall Murphy
- & James C. W. Locke
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Article
| Open AccessFoxg specifies sensory neurons in the anterior neural plate border of the ascidian embryo
Vertebrate telencephalon formation requires Foxg-Fgf8 cross-regulation, but while ascidians express Foxg in the neural plate, they lack a telencephalon. Here the authors show that Foxg loss does not affect ascidian brain formation, indicating that telencephalon evolution required recruitment of Fgf downstream of Foxg.
- Boqi Liu
- & Yutaka Satou
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Article
| Open AccessCell competition corrects noisy Wnt morphogen gradients to achieve robust patterning in the zebrafish embryo
Gradients of morphogens such as Wnt provide instructive cues for cell identities during development. Here, the authors report that in the developing zebrafish embryo, cell competition and elimination of unfit cells are required for proper Wnt gradient formation.
- Yuki Akieda
- , Shohei Ogamino
- & Tohru Ishitani
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Article
| Open AccessMaternal pluripotency factors initiate extensive chromatin remodelling to predefine first response to inductive signals
Embryonic development produces different cell types in response to a small number of inductive signals. Here, the authors characterise how maternal factors modify chromatin to specify initial competence in Xenopus tropicalis, finding that the pioneering activity of the pluripotency factors Pou5f3 and Sox3 establishes competence for germ layer formation by remodelling chromatin before the onset of signalling.
- George E. Gentsch
- , Thomas Spruce
- & James C. Smith
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Article
| Open AccessIn vivo Hox binding specificity revealed by systematic changes to a single cis regulatory module
Hox proteins are expressed in partially overlapping regions to inform development along the embryo’s head-tail axis. Here the authors analyse a cis regulatory module directly regulated by seven different Drosophila Hox proteins to uncover how different Hox class proteins differentially control its expression.
- Carlos Sánchez-Higueras
- , Chaitanya Rastogi
- & James C.-G. Hombría
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Article
| Open AccessRegulation of Notch output dynamics via specific E(spl)-HLH factors during bristle patterning in Drosophila
The patterning of sensory bristles on the dorsal thorax of flies is regulated by two transcription factor families but the dynamics of this regulation is unclear. Here, the authors visualize seven E(spl)-HLH proteins, showing their regulated expression promotes mutual inhibition by Notch during notum patterning.
- Lydie Couturier
- , Khalil Mazouni
- & François Schweisguth
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Article
| Open AccessMechanical impact of epithelial−mesenchymal transition on epithelial morphogenesis in Drosophila
Tissue folding is a critical process during developmental morphogenesis. Here, Gracia et al. use live imaging, laser ablation and in silico modelling to demonstrate that cells entering EMT generate orthogonal forces necessary to drive mesoderm invagination in Drosophila.
- Mélanie Gracia
- , Sophie Theis
- & Magali Suzanne
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Article
| Open AccessMuscle functions as a connective tissue and source of extracellular matrix in planarians
How the cellular source of positional information compares across regenerative animals is unclear. Here, the authors find that planarian muscle, which harbours positional information, acts as a connective tissue by being a major site of matrisome gene expression and by maintaining tissue architecture.
- Lauren E. Cote
- , Eric Simental
- & Peter W. Reddien
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Article
| Open AccessSynthetic mammalian pattern formation driven by differential diffusivity of Nodal and Lefty
Nodal-Lefty signaling combines a short-range activator and a long-range inhibitor for axis formation and left-right patterning. Here the authors reconstitute a synthetic biology activator-inhibitor circuit of Nodal-Lefty to drive pattern formation in mammalian cells.
- Ryoji Sekine
- , Tatsuo Shibata
- & Miki Ebisuya
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Article
| Open AccessDynamic intercellular transport modulates the spatial patterning of differentiation during early neural commitment
How heterogeneities arise in stem cell populations remains unclear. Here, Glen et al. find that in ESC colonies cell cycle asynchronies modulate gap junctions, causing variation in intracellular signalling molecule diffusion between cells, and ultimately in spatial heterogeneity in differentiation.
- Chad M. Glen
- , Todd C. McDevitt
- & Melissa L. Kemp
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Article
| Open AccessIridophores as a source of robustness in zebrafish stripes and variability in Danio patterns
Iridophores interact with other cells to give zebrafish their stripes, but what drives their form shifts is unknown. Here, modelling allows the authors to identify robust cues that may specify iridophore form and to find changes to these cues that likely account for altered patterns on related fish.
- Alexandria Volkening
- & Björn Sandstede
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Comment
| Open AccessMaking head or tail of cnidarian hox gene function
Hox genes are known to regulate head-tail axis patterning but their molecular role in animals diverged from the bilaterian lineage is unclear. Here, Fabian Rentzsch and Thomas W. Holstein comment on a paper by Mark Martindale and colleagues on the functional role of two Hox genes in axial patterning of the sea anemone.
- Fabian Rentzsch
- & Thomas W. Holstein
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Article
| Open AccessMyosin1D is an evolutionarily conserved regulator of animal left–right asymmetry
Left-right (LR) axis specification is essential for embryonic patterning but a unifying mechanism across organisms has not been identified. Here, the authors show that Myosin1D, known to regulate Drosophila LR asymmetry, controls zebrafish LR Organizer function, and is therefore a conserved regulator of animal laterality.
- Thomas Juan
- , Charles Géminard
- & Maximilian Fürthauer
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Perspective
| Open AccessTracing the origin of heterogeneity and symmetry breaking in the early mammalian embryo
What breaks symmetry in early mammalian embryonic development has been much questioned. Here, Magdalena Zernicka-Goetz and colleagues propose that compartmentalized intracellular reactions generate micro-scale inhomogeneity, which is amplified in the developing embryo, driving pattern formation.
- Qi Chen
- , Junchao Shi
- & Magdalena Zernicka-Goetz
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Article
| Open AccessProgrammed hierarchical patterning of bacterial populations
Biological self-organization uses hierarchical induction of gene expression but this has not been exploited by synthetic biology. Here the authors use an AND gate based on a split T7 RNA polymerase to organize programmed hierarchical patterning of gene expression across a bacterial population.
- Christian R. Boehm
- , Paul K. Grant
- & Jim Haseloff
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Article
| Open AccessSelf-patterning of rostral-caudal neuroectoderm requires dual role of Fgf signaling for localized Wnt antagonism
The neuroectoderm is patterned in a rostral-caudal axis in the embryo but how positional information is interpreted, is unclear. Here, the authors show that in mouse 3D embryonic stem cell cultures, there is self-patterning that depends on sequential activation of localised Fgf then Wnt signalling.
- Nozomu Takata
- , Eriko Sakakura
- & Yoshiki Sasai
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Article
| Open AccessAcoel regeneration mechanisms indicate an ancient role for muscle in regenerative patterning
Planarian regenerative mechanisms suggest that muscle has an instructive role in patterning. Here, the authors show that muscle is also responsible for regenerative patterning information in an early-branching bilaterian, Hofstenia miamia, dating this back to the dawn of the Bilateria, over 550 million years ago.
- Amelie A. Raz
- , Mansi Srivastava
- & Peter W. Reddien
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Article
| Open AccessThe WHHERE coactivator complex is required for retinoic acid-dependent regulation of embryonic symmetry
Retinoic acid (RA) regulates the maintenance of somitogenesis symmetry. Here, the authors use a proteomic approach to identify a protein complex of Wdr5, Hdac1, Hdac2 that act together with RA and coactivator Rere/Atrophin2 and a histone methyltransferase Ehmt2 to regulate embryonic symmetry.
- Gonçalo C. Vilhais-Neto
- , Marjorie Fournier
- & Olivier Pourquié
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Article
| Open AccessPervasive translational regulation of the cell signalling circuitry underlies mammalian development
Gene expression is regulated at several levels, including through the modulation of protein translation. Here the authors find that translation control diversifies gene expression between developing tissues and regulates major signalling pathways through a complex landscape of upstream open reading frames (uORFs).
- Kotaro Fujii
- , Zhen Shi
- & Maria Barna
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Article
| Open AccessDiverse feather shape evolution enabled by coupling anisotropic signalling modules with self-organizing branching programme
Asymmetric feather vane shape was a critical innovation in feather evolution and adaptation for flight. Here, Li and colleagues characterize the multi-module regulatory network that controls feather vane shape and underlies feather diversification.
- Ang Li
- , Seth Figueroa
- & Cheng-Ming Chuong
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Article
| Open AccessBulk cell density and Wnt/TGFbeta signalling regulate mesendodermal patterning of human pluripotent stem cells
Differentiation of human pluripotent stem cells (hPSC) mimics aspects of embryonic developmentin vitrobut is poorly understood. Here, the authors identify bulk cell density as a key parameter directing transition from pluripotency to primitive streak-like priming in hPSCs via secreted LEFTY/CERBERUS.
- Henning Kempf
- , Ruth Olmer
- & Robert Zweigerdt
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Article
| Open AccessAn interdigit signalling centre instructs coordinate phalanx-joint formation governed by 5′Hoxd–Gli3 antagonism
The molecular mechanisms governing digit joint specification are poorly understood. Here, the authors identify the 5′Hoxd–Gli3 balance as a key regulator of the net interdigital Bmp signalling level in mouse, which in turn regulates phalanx and joint formation.
- Bau-Lin Huang
- , Anna Trofka
- & Susan Mackem
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Article
| Open AccessA strategy to discover new organizers identifies a putative heart organizer
Organizers are regions in the embryo that induce cell fate and impart pattern on neighbouring regions. Here, the authors search for new organizers based on a common gene signature, and show that the Anterior Intestinal Portal endoderm induces cardiac identity, specifies ventricle and inhibits atrial character.
- Claire Anderson
- , Mohsin A. F. Khan
- & Claudio D. Stern
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Article
| Open AccessSelf-organized centripetal movement of corneal epithelium in the absence of external cues
The cornea is formed of cells that originate from the outer circle of stem cells and that move towards its centre. Here, the authors show that the movement pattern is self-organised, requiring no cues, and that stem cell leakage may account for the presence of stem cells at the centre of the cornea.
- Erwin P. Lobo
- , Naomi C. Delic
- & J. Guy Lyons
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Article
| Open AccessBMP and retinoic acid regulate anterior–posterior patterning of the non-axial mesoderm across the dorsal–ventral axis
It is unclear how the dorsal-ventral (DV) and anterior-posterior (AP) axes established in the gastrula affect tissues. Here, the authors show that in zebrafish kidney development, with regard to non-axial mesoderm, the classic DV axis corresponds to the AP axis, and is regulated by BMP and retinoic acid.
- Richard W. Naylor
- , Lauren Brilli Skvarca
- & Alan J. Davidson
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Article
| Open AccessHomotypic cell competition regulates proliferation and tiling of zebrafish pigment cells during colour pattern formation
Melanophores, iridophores and xanthophores are pigment-cell types that interact to form the stripes in zebrafish. Here, the authors study the interaction between cells of the same kind and show that each pigment-cell type covers the skin by contact based competition.
- Brigitte Walderich
- , Ajeet Pratap Singh
- & Christiane Nüsslein-Volhard
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Article
| Open AccessPeriodic patterning of the Drosophila eye is stabilized by the diffusible activator Scabrous
Patterning in the Drosophila eye is achieved by a series of signalling cascades over several cell distances. Here Gavish et al.model lateral inhibition in the developing eye to understand how developmental noise refines such patterning, identifying a novel activator required for buffering spatial variability.
- Avishai Gavish
- , Arkadi Shwartz
- & Naama Barkai
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Article
| Open AccessTorso-like mediates extracellular accumulation of Furin-cleaved Trunk to pattern the Drosophila embryo termini
Activation of the growth factor Trunk patterns the Drosophila embryonic termini but how this is regulated is unclear. Here, Johnson et al.report that Trunk is cleaved intracellularly by Furin proteases, and its extracellular accumulation is then mediated by the perforin-like protein Torso-like.
- Travis K. Johnson
- , Michelle A. Henstridge
- & Coral G. Warr
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Article
| Open AccessPigment cell movement is not required for generation of Turing patterns in zebrafish skin
Pigment pattern formation in zebrafish depends on the interactions between the pigment cells. Here the authors present a mathematical model based on mutual interaction of pigment cells in the absence of cell motion, revising the current model of the pattern formation that relies on reaction–diffusion Turing patterns.
- D. Bullara
- & Y. De Decker
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Article |
Shared rules of development predict patterns of evolution in vertebrate segmentation
Despite apparent morphological diversity, developmental interactions create predictable patterns of variation. Here the authors show that variation in the proportion of limbs, digits and somites and their response to artificial selection follow a rule that predicts the size of sequentially forming structures.
- Nathan M. Young
- , Benjamin Winslow
- & Kathryn Kavanagh
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Article |
Fundamental origins and limits for scaling a maternal morphogen gradient
Maternal molecular resources are invested in an egg so that different parts of the future embryo are specified and scaled in proportion to its size. Here the authors develop and experimentally test a model that evaluates the origins and limits of Bicoid morphogenetic gradient scaling in the fruit fly embryo.
- Feng He
- , Chuanxian Wei
- & Jun Ma
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Article |
HEB associates with PRC2 and SMAD2/3 to regulate developmental fates
In embryonic stem cells, extracellular signals are required to derepress developmental promoters to drive lineage specification, but the proteins involved in this process remain unknown. Here the authors show that the protein HEB directly associates with the Polycomb repressive complex 2 at genes involved in mesoderm and endoderm specification.
- Se-Jin Yoon
- , Joseph W. Foley
- & Julie C. Baker
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Article |
Primitive macrophages control HSPC mobilization and definitive haematopoiesis
Haematopoietic stem/progenitor cells (HSPCs) transform from aortic endothelium into migratory cells that move through stroma and enter circulation to colonize haematopoietic tissues. Here the authors show that HSPCs' passage is facilitated by primitive macrophages that secrete extracellular matrix-degrading enzymes.
- Jana Travnickova
- , Vanessa Tran Chau
- & Karima Kissa
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Article |
PFKFB4 controls embryonic patterning via Akt signalling independently of glycolysis
PFKFB4 is an enzyme known to regulate glycolysis. The authors reveal a surprising new role for this protein in global patterning of dorsal ectoderm in frogs that is mediated by Akt signalling and independent of glycolysis.
- Caterina Pegoraro
- , Ana Leonor Figueiredo
- & Anne H. Monsoro-Burq
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Article
| Open AccessFibroblast growth factor signalling controls nervous system patterning and pigment cell formation in Ciona intestinalis
The fibroblast growth factor (FGF) signalling pathway specifies the fate of pigmented cells in the ascidian Ciona intestinalis. Here, the authors obtain lineage-specific transcription profiles of pigment precursor cells and identify FGF downstream genes involved in central nervous system patterning, and the specification and differentiation of pigmented cells.
- Claudia Racioppi
- , Ashwani K. Kamal
- & Filomena Ristoratore
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Article
| Open AccessCdon acts as a Hedgehog decoy receptor during proximal-distal patterning of the optic vesicle
The Drosophilahomologue of the vertebrate cell surface glycoprotein Cdon binds Hedgehog ligand and thereby prevents its diffusion. Here, the authors provide evidence for a similar mechanism during vertebrate optic vesicle patterning, where Cdon acts as a negative regulator of Hedgehog signalling to define the boundary between the optic stalk and the retina.
- Marcos Julián Cardozo
- , Luisa Sánchez-Arrones
- & Paola Bovolenta
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Article
| Open AccessOrganizer-derived Bmp2 is required for the formation of a correct Bmp activity gradient during embryonic development
The morphogen, Bmp, regulates differentiation of cell fates along the ventral to dorsal axis during vertebrate embryonic development. Here, Xue et al. show that Bmp2b produced by the organizer during early gastrulation in zebrafish embryos has a role in the establishment of an appropriate Bmp morphogen activity gradient and the correct dorsoventral patterning of the embryos.
- Yu Xue
- , Xiudeng Zheng
- & Anming Meng
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Article |
Trunk cleavage is essential for Drosophila terminal patterning and can occur independently of Torso-like
Terminal patterning of the Drosophila embryo is thought to be regulated by local cleavage of the ubiquitous peptide hormone Trunk (Trk) controlled by the maternal gene torso-like (tsl)that is expressed only at embryo poles. Here, the authors show that cleavage of Trk is indeed required for patterning and can occur independently of Tsl.
- Michelle A. Henstridge
- , Travis K. Johnson
- & James C. Whisstock
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Article |
Lysine-specific demethylase 1 regulates differentiation onset and migration of trophoblast stem cells
The histone demethylase Lsd1 regulates the balance between self-renewal and differentiation in human embryonic stem cells. Here, the authors show that the loss of Lsd1 in the trophectoderm of mouse embryos leads to premature differentiation of trophoblast stem cells, partially due to de-repression of the transcription factor Ovol2.
- Dongmei Zhu
- , Stefanie Hölz
- & Roland Schüle
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Article |
Dampened regulates the activating potency of Bicoid and the embryonic patterning outcome in Drosophila
The morphogen Bicoid regulates anterior–posterior patterning in the early Drosophila embryo by locally activating its target genes such as hunchback. Here, the authors identify the F-box protein Dampened as a regulator of Bicoid-dependent transcriptional activation of hunchback.
- Junbo Liu
- & Jun Ma
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Article |
Insights into bird wing evolution and digit specification from polarizing region fate maps
Bird wings resemble the digits on the hands of dinosaurs, but which digit positions gave rise to those seen in modern birds is still unclear. In this work, long-term fate maps of the chick wing polarizing region are presented, supporting fossil data that birds descended from theropods that had digits 1, 2 and 3.
- Matthew Towers
- , Jason Signolet
- & Cheryll Tickle
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Article
| Open AccessIdentification of vertebra-like elements and their possible differentiation from sclerotomes in the hagfish
Hagfish, a group of extant jawless fish, lack true vertebrae, but it is not clear if hagfish lack all vertebrata-like structures. Here the authors report the presence of vertebra-like cartilages in the in-shore hagfish, suggesting that the hagfish underwent secondary reduction of vertebra.
- Kinya G. Ota
- , Satoko Fujimoto
- & Shigeru Kuratani