In vertebrates, head and trunk muscles develop from different mesodermal populations and are regulated by distinct genetic networks. Neck muscles at the head-trunk interface remain poorly defined due to their complex morphogenesis and dual mesodermal origins. Here, we use genetically modified mice to establish a 3D model that integrates regulatory genes, cell populations and morphogenetic events that define this transition zone. We show that the evolutionary conserved cucullaris-derived muscles originate from posterior cardiopharyngeal mesoderm, not lateral plate mesoderm, and we define new boundaries for neural crest and mesodermal contributions to neck connective tissue. Furthermore, lineage studies and functional analysis of Tbx1- and Pax3-null mice reveal a unique developmental program for somitic neck muscles that is distinct from that of somitic trunk muscles. Our findings unveil the embryological and developmental requirements underlying tetrapod neck myogenesis and provide a blueprint to investigate how muscle subsets are selectively affected in some human myopathies.

Aix Marseille Université CNRS UMR 7288 IBDM Marseille France

Central European Institute of Technology Brno University of Technology Brno Czech Republic

CNRS UMR 3738 Paris France

Department of Developmental and Stem Cell Biology Institut Pasteur Paris France

Department of Human Genetics University of Utah Salt Lake City United States

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Adachi N, Pascual-Anaya J, Hirai T, Higuchi S, Kuratani S. Development of hypobranchial muscles with special reference to the evolution of the vertebrate neck. Zoological Letters. 2018;4:5. doi: 10.1186/s40851-018-0087-x. PubMed DOI PMC

Arnold JS, Werling U, Braunstein EM, Liao J, Nowotschin S, Edelmann W, Hebert JM, Morrow BE. Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development. 2006;133:977–987. doi: 10.1242/dev.02264. PubMed DOI

Brown CB, Engleka KA, Wenning J, Min Lu M, Epstein JA. Identification of a hypaxial somite enhancer element regulating Pax3 expression in migrating myoblasts and characterization of hypaxial muscle Cre transgenic mice. Genesis. 2005;41:202–209. doi: 10.1002/gene.20116. PubMed DOI

Burke AC, Nowicki JL. A new view of patterning domains in the vertebrate mesoderm. Developmental Cell. 2003;4:159–165. doi: 10.1016/S1534-5807(03)00033-9. PubMed DOI

Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, Chen J, Evans S. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Developmental Cell. 2003;5:877–889. doi: 10.1016/S1534-5807(03)00363-0. PubMed DOI PMC

Comai G, Sambasivan R, Gopalakrishnan S, Tajbakhsh S. Variations in the efficiency of lineage marking and ablation confound distinctions between myogenic cell populations. Developmental Cell. 2014;31:654–667. doi: 10.1016/j.devcel.2014.11.005. PubMed DOI

Comai G, Tajbakhsh S. Molecular and cellular regulation of skeletal myogenesis. Current Topics in Developmental Biology. 2014;110:1–73. doi: 10.1016/B978-0-12-405943-6.00001-4. PubMed DOI

Couly GF, Coltey PM, Le Douarin NM. The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development. 1993;117:409–429. PubMed

Danielian PS, Muccino D, Rowitch DH, Michael SK, McMahon AP. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Current Biology. 1998;8:1323–S2. doi: 10.1016/S0960-9822(07)00562-3. PubMed DOI

Diogo RA. Muscles of Vertebrates - Comparative Anatomy, Evolution, Homologies and Development. Enfield, New Hampshire: Science Publishers; 2010. DOI

Diogo R, Kelly RG, Christiaen L, Levine M, Ziermann JM, Molnar JL, Noden DM, Tzahor E. A new heart for a new head in vertebrate cardiopharyngeal evolution. Nature. 2015;520:466–473. doi: 10.1038/nature14435. PubMed DOI PMC

Durland JL, Sferlazzo M, Logan M, Burke AC. Visualizing the lateral somitic frontier in the Prx1Cre transgenic mouse. Journal of Anatomy. 2008;212:590–602. doi: 10.1111/j.1469-7580.2008.00879.x. PubMed DOI PMC

Edgeworth FH. The Cranial Muscles of Vertebrates. Cambridge University Press; 1935.

Emery AEH. The muscular dystrophies. The Lancet. 2002;359:687–695. doi: 10.1016/S0140-6736(02)07815-7. PubMed DOI

Engleka KA, Gitler AD, Zhang M, Zhou DD, High FA, Epstein JA. Insertion of Cre into the Pax3 locus creates a new allele of Splotch and identifies unexpected Pax3 derivatives. Developmental Biology. 2005;280:396–406. doi: 10.1016/j.ydbio.2005.02.002. PubMed DOI

Epperlein HH, Khattak S, Knapp D, Tanaka EM, Malashichev YB. Neural crest does not contribute to the neck and shoulder in the axolotl (Ambystoma mexicanum) PLOS ONE. 2012;7:e52244. doi: 10.1371/journal.pone.0052244. PubMed DOI PMC

Ericsson R, Knight R, Johanson Z. Evolution and development of the vertebrate neck. Journal of Anatomy. 2013;222:67–78. doi: 10.1111/j.1469-7580.2012.01530.x. PubMed DOI PMC

Evans DJ, Noden DM. Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells. Developmental Dynamics. 2006;235:1310–1325. doi: 10.1002/dvdy.20663. PubMed DOI

Gopalakrishnan S, Comai G, Sambasivan R, Francou A, Kelly RG, Tajbakhsh S. A Cranial Mesoderm Origin for Esophagus Striated Muscles. Developmental Cell. 2015;34:694–704. doi: 10.1016/j.devcel.2015.07.003. PubMed DOI

Greil A. Entwicklungsgeschichte des Kopfes und des Blutgefässsystemes von Ceratodus forsteri. II. Die epigenetischen Erwerbungen während der Stadien 39–48. Denkschr Med-Naturwiss Ges Jena. Denkschriften Der Medicinisch-NaturwissenschaftlichenGesellschaft Zu Jena. 1913;9:935–1492.

Grifone R, Jarry T, Dandonneau M, Grenier J, Duprez D, Kelly RG. Properties of branchiomeric and somite-derived muscle development in Tbx1 mutant embryos. Developmental Dynamics. 2008;237:3071–3078. doi: 10.1002/dvdy.21718. PubMed DOI

Haldar M, Hancock JD, Coffin CM, Lessnick SL, Capecchi MR. A conditional mouse model of synovial sarcoma: insights into a myogenic origin. Cancer Cell. 2007;11:375–388. doi: 10.1016/j.ccr.2007.01.016. PubMed DOI

Hamidi M, Nabi S, Husein M, Mohamed ME, Tay KY, McKillop S. Cervical spine abnormalities in 22q11.2 deletion syndrome. The Cleft Palate-Craniofacial Journal. 2014;51:230–233. doi: 10.1597/12-318. PubMed DOI

Hanken J, Gross JB. Evolution of cranial development and the role of neural crest: insights from amphibians. Journal of Anatomy. 2005;207:437–446. doi: 10.1111/j.1469-7580.2005.00481.x. PubMed DOI PMC

Haraguchi S, Kitajima S, Takagi A, Takeda H, Inoue T, Saga Y. Transcriptional regulation of Mesp1 and Mesp2 genes: differential usage of enhancers during development. Mechanisms of Development. 2001;108:59–69. doi: 10.1016/S0925-4773(01)00478-6. PubMed DOI

Harel I, Nathan E, Tirosh-Finkel L, Zigdon H, Guimarães-Camboa N, Evans SM, Tzahor E. Distinct origins and genetic programs of head muscle satellite cells. Developmental Cell. 2009;16:822–832. doi: 10.1016/j.devcel.2009.05.007. PubMed DOI PMC

Huang R, Zhi Q, Ordahl CP, Christ B. The fate of the first avian somite. Anatomy and Embryology. 1997;195:435–449. doi: 10.1007/s004290050063. PubMed DOI

Huang R, Zhi Q, Patel K, Wilting J, Christ B. Contribution of single somites to the skeleton and muscles of the occipital and cervical regions in avian embryos. Anatomy and Embryology. 2000;202:375–383. doi: 10.1007/s004290000131. PubMed DOI

Huynh T, Chen L, Terrell P, Baldini A. A fate map of Tbx1 expressing cells reveals heterogeneity in the second cardiac field. Genesis. 2007;45:470–475. doi: 10.1002/dvg.20317. PubMed DOI

Jerome LA, Papaioannou VE. DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nature Genetics. 2001;27:286–291. doi: 10.1038/85845. PubMed DOI

Kague E, Gallagher M, Burke S, Parsons M, Franz-Odendaal T, Fisher S. Skeletogenic fate of zebrafish cranial and trunk neural crest. PLOS ONE. 2012;7:e47394. doi: 10.1371/journal.pone.0047394. PubMed DOI PMC

Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomès D, Tajbakhsh S. Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes & Development. 2005;19:1426–1431. doi: 10.1101/gad.345505. PubMed DOI PMC

Kelly RG, Jerome-Majewska LA, Papaioannou VE. The del22q11.2 candidate gene Tbx1 regulates branchiomeric myogenesis. Human Molecular Genetics. 2004;13:2829–2840. doi: 10.1093/hmg/ddh304. PubMed DOI

Kong P, Racedo SE, Macchiarulo S, Hu Z, Carpenter C, Guo T, Wang T, Zheng D, Morrow BE. Tbx1 is required autonomously for cell survival and fate in the pharyngeal core mesoderm to form the muscles of mastication. Human Molecular Genetics. 2014;23:4215–4231. doi: 10.1093/hmg/ddu140. PubMed DOI PMC

Köntges G, Lumsden A. Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development. 1996;122:3229–3242. PubMed

Kuratani S. Evolutionary developmental studies of cyclostomes and the origin of the vertebrate neck. Development, Growth & Differentiation. 2008;50:S189–S194. doi: 10.1111/j.1440-169X.2008.00985.x. PubMed DOI

Kuratani S, Kusakabe R, Hirasawa T. The neural crest and evolution of the head/trunk interface in vertebrates. Developmental Biology. 2018 doi: 10.1016/j.ydbio.2018.01.017. PubMed DOI

Leopold C, De Barros A, Cellier C, Drouin-Garraud V, Dehesdin D, Marie JP. Laryngeal abnormalities are frequent in the 22q11 deletion syndrome. International Journal of Pediatric Otorhinolaryngology. 2012;76:36–40. doi: 10.1016/j.ijporl.2011.09.025. PubMed DOI

Lescroart F, Kelly RG, Le Garrec JF, Nicolas JF, Meilhac SM, Buckingham M. Clonal analysis reveals common lineage relationships between head muscles and second heart field derivatives in the mouse embryo. Development. 2010;137:3269–3279. doi: 10.1242/dev.050674. PubMed DOI

Lescroart F, Hamou W, Francou A, Théveniau-Ruissy M, Kelly RG, Buckingham M. Clonal analysis reveals a common origin between nonsomite-derived neck muscles and heart myocardium. PNAS. 2015;112:1446–1451. doi: 10.1073/pnas.1424538112. PubMed DOI PMC

Loebel DA, Hor AC, Bildsoe H, Jones V, Chen YT, Behringer RR, Tam PP. Regionalized Twist1 activity in the forelimb bud drives the morphogenesis of the proximal and preaxial skeleton. Developmental Biology. 2012;362:132–140. doi: 10.1016/j.ydbio.2011.11.020. PubMed DOI

Logan M, Martin JF, Nagy A, Lobe C, Olson EN, Tabin CJ. Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis. 2002;33:77–80. doi: 10.1002/gene.10092. PubMed DOI

Lours-Calet C, Alvares LE, El-Hanfy AS, Gandesha S, Walters EH, Sobreira DR, Wotton KR, Jorge EC, Lawson JA, Kelsey Lewis A, Tada M, Sharpe C, Kardon G, Dietrich S. Evolutionarily conserved morphogenetic movements at the vertebrate head-trunk interface coordinate the transport and assembly of hypopharyngeal structures. Developmental Biology. 2014;390:231–246. doi: 10.1016/j.ydbio.2014.03.003. PubMed DOI PMC

Lubosch W. Muskeln des Kopfes: Viscerale Muskulatur. In: Bolk L, Göppert E, Kallius E, Lubosch W, editors. Handbuch Der Vergleichenden Anatomie Der Wirbeltiere. Berlin: Urban & Schwarzenberg; 1938.

Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nature Neuroscience. 2010;13:133–140. doi: 10.1038/nn.2467. PubMed DOI PMC

Marom T, Roth Y, Goldfarb A, Cinamon U. Head and neck manifestations of 22q11.2 deletion syndromes. European Archives of Oto-Rhino-Laryngology. 2012;269:381–387. doi: 10.1007/s00405-011-1745-1. PubMed DOI

Martin AR, Reddy R, Fehlings MG. Dropped head syndrome: diagnosis and management. Evidence-Based Spine-Care Journal. 2011;2:41–47. doi: 10.1055/s-0030-1267104. PubMed DOI PMC

Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, Richardson WD, McMahon AP, Koentges G. Neural crest origins of the neck and shoulder. Nature. 2005;436:347–355. doi: 10.1038/nature03837. PubMed DOI PMC

McGonnell IM, McKay IJ, Graham A. A population of caudally migrating cranial neural crest cells: functional and evolutionary implications. Developmental Biology. 2001;236:354–363. doi: 10.1006/dbio.2001.0330. PubMed DOI

Moreno TA, Jappelli R, Izpisúa Belmonte JC, Kintner C. Retinoic acid regulation of the Mesp-Ripply feedback loop during vertebrate segmental patterning. Developmental Biology. 2008;315:317–330. doi: 10.1016/j.ydbio.2007.12.038. PubMed DOI PMC

Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis. 2007;45:593–605. doi: 10.1002/dvg.20335. PubMed DOI

Nagashima H, Sugahara F, Watanabe K, Shibata M, Chiba A, Sato N. Developmental origin of the clavicle, and its implications for the evolution of the neck and the paired appendages in vertebrates. Journal of Anatomy. 2016;229:536–548. doi: 10.1111/joa.12502. PubMed DOI PMC

Nassari S, Duprez D, Fournier-Thibault C. Non-myogenic Contribution to Muscle Development and Homeostasis: The Role of Connective Tissues. Frontiers in Cell and Developmental Biology. 2017;5:22. doi: 10.3389/fcell.2017.00022. PubMed DOI PMC

Nathan E, Monovich A, Tirosh-Finkel L, Harrelson Z, Rousso T, Rinon A, Harel I, Evans SM, Tzahor E. The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development. Development. 2008;135:647–657. doi: 10.1242/dev.007989. PubMed DOI PMC

Naumann B, Warth P, Olsson L, Konstantinidis P. The development of the cucullaris muscle and the branchial musculature in the Longnose Gar, (Lepisosteus osseus, Lepisosteiformes, Actinopterygii) and its implications for the evolution and development of the head/trunk interface in vertebrates. Evolution & Development. 2017;19:263–276. doi: 10.1111/ede.12239. PubMed DOI

Noda M, Miyake T, Okabe M. Development of cranial muscles in the actinopterygian fish Senegal bichir, Polypterus senegalus Cuvier, 1829. Journal of Morphology. 2017;278:450–463. doi: 10.1002/jmor.20636. PubMed DOI

Noden DM. The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. American Journal of Anatomy. 1983;168:257–276. doi: 10.1002/aja.1001680302. PubMed DOI

Noden DM. Interactions and fates of avian craniofacial mesenchyme. Development. 1988;103:121–140. PubMed

Noden DM, Francis-West P. The differentiation and morphogenesis of craniofacial muscles. Developmental Dynamics. 2006;235:1194–1218. doi: 10.1002/dvdy.20697. PubMed DOI

Okano J, Sakai Y, Shiota K. Retinoic acid down-regulates Tbx1 expression and induces abnormal differentiation of tongue muscles in fetal mice. Developmental Dynamics. 2008;237:3059–3070. doi: 10.1002/dvdy.21715. PubMed DOI

Olsson L, Falck P, Lopez K, Cobb J, Hanken J. Cranial neural crest cells contribute to connective tissue in cranial muscles in the anuran amphibian, Bombina orientalis. Developmental Biology. 2001;237:354–367. doi: 10.1006/dbio.2001.0377. PubMed DOI

Papangeli I, Scambler P. The 22q11 deletion: DiGeorge and velocardiofacial syndromes and the role of TBX1. Wiley Interdisciplinary Reviews: Developmental Biology. 2013;2:393–403. doi: 10.1002/wdev.75. PubMed DOI

Parameswaran M, Tam PP. Regionalisation of cell fate and morphogenetic movement of the mesoderm during mouse gastrulation. Developmental Genetics. 1995;17:16–28. doi: 10.1002/dvg.1020170104. PubMed DOI

Piatt J. Morphogenesis of the cranial muscles of Amblystoma punctatum. Journal of Morphology. 1938;63:531–587. doi: 10.1002/jmor.1050630306. DOI

Piekarski N, Gross JB, Hanken J. Evolutionary innovation and conservation in the embryonic derivation of the vertebrate skull. Nature Communications. 2014;5:5661. doi: 10.1038/ncomms6661. PubMed DOI PMC

Piekarski N, Olsson L. Muscular derivatives of the cranialmost somites revealed by long-term fate mapping in the Mexican axolotl (Ambystoma mexicanum) Evolution & Development. 2007;9:566–578. doi: 10.1111/j.1525-142X.2007.00197.x. PubMed DOI

Ponomartsev S, Valasek P, Patel K, Malashichev Y. Neural crest contribution to the avian shoulder girdle and implications to girdle evolution in vertebrates. Biological Communications. 2017;62:26–37. doi: 10.21638/11701/spbu03.2017.104. DOI

Prunotto C, Crepaldi T, Forni PE, Ieraci A, Kelly RG, Tajbakhsh S, Buckingham M, Ponzetto C. Analysis of Mlc-lacZ Met mutants highlights the essential function of Met for migratory precursors of hypaxial muscles and reveals a role for Met in the development of hyoid arch-derived facial muscles. Developmental Dynamics. 2004;231:582–591. doi: 10.1002/dvdy.20177. PubMed DOI

Randolph ME, Pavlath GK. A muscle stem cell for every muscle: variability of satellite cell biology among different muscle groups. Frontiers in Aging Neuroscience. 2015;7:190. doi: 10.3389/fnagi.2015.00190. PubMed DOI PMC

Relaix F, Rocancourt D, Mansouri A, Buckingham M. Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes & Development. 2004;18:1088–1105. doi: 10.1101/gad.301004. PubMed DOI PMC

Relaix F, Rocancourt D, Mansouri A, Buckingham M. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature. 2005;435:948–953. doi: 10.1038/nature03594. PubMed DOI

Saga Y, Hata N, Kobayashi S, Magnuson T, Seldin MF, Taketo MM. MesP1: a novel basic helix-loop-helix protein expressed in the nascent mesodermal cells during mouse gastrulation. Development. 1996;122:2769–2778. PubMed

Saga Y. Genetic rescue of segmentation defect in MesP2-deficient mice by MesP1 gene replacement. Mechanisms of Development. 1998;75:53–66. doi: 10.1016/S0925-4773(98)00077-X. PubMed DOI

Saga Y, Miyagawa-Tomita S, Takagi A, Kitajima S, Miyazaki J, Inoue T. MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development. 1999;126:3437–3447. PubMed

Saga Y, Kitajima S, Miyagawa-Tomita S. Mesp1 expression is the earliest sign of cardiovascular development. Trends in Cardiovascular Medicine. 2000;10:345–352. doi: 10.1016/S1050-1738(01)00069-X. PubMed DOI

Sambasivan R, Gayraud-Morel B, Dumas G, Cimper C, Paisant S, Kelly RG, Kelly R, Tajbakhsh S. Distinct regulatory cascades govern extraocular and pharyngeal arch muscle progenitor cell fates. Developmental Cell. 2009;16:810–821. doi: 10.1016/j.devcel.2009.05.008. PubMed DOI

Sambasivan R, Comai G, Le Roux I, Gomès D, Konge J, Dumas G, Cimper C, Tajbakhsh S. Embryonic founders of adult muscle stem cells are primed by the determination gene Mrf4. Developmental Biology. 2013;381:241–255. doi: 10.1016/j.ydbio.2013.04.018. PubMed DOI

Satou Y, Imai KS, Satoh N. The ascidian Mesp gene specifies heart precursor cells. Development. 2004;131:2533–2541. doi: 10.1242/dev.01145. PubMed DOI

Sawada A, Fritz A, Jiang YJ, Yamamoto A, Yamasu K, Kuroiwa A, Saga Y, Takeda H. Zebrafish Mesp family genes, mesp-a and mesp-b are segmentally expressed in the presomitic mesoderm, and Mesp-b confers the anterior identity to the developing somites. Development. 2000;127:1691–1702. PubMed

Sefton EM, Bhullar BA, Mohaddes Z, Hanken J. Evolution of the head-trunk interface in tetrapod vertebrates. eLife. 2016;5:e09972. doi: 10.7554/eLife.09972. PubMed DOI PMC

Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genetics. 1999;21:70–71. doi: 10.1038/5007. PubMed DOI

Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Developmental Biology. 2001;1:4. PubMed PMC

Tabler JM, Rigney MM, Berman GJ, Gopalakrishnan S, Heude E, Al-Lami HA, Yannakoudakis BZ, Fitch RD, Carter C, Vokes S, Liu KJ, Tajbakhsh S, Egnor SR, Wallingford JB. Cilia-mediated Hedgehog signaling controls form and function in the mammalian larynx. eLife. 2017;6:e19153. doi: 10.7554/eLife.19153. PubMed DOI PMC

Tada MN, Kuratani S. Evolutionary and developmental understanding of the spinal accessory nerve. Zoological Letters. 2015;1:4. doi: 10.1186/s40851-014-0006-8. PubMed DOI PMC

Tajbakhsh S, Rocancourt D, Buckingham M. Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice. Nature. 1996;384:266–270. doi: 10.1038/384266a0. PubMed DOI

Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell. 1997;89:127–138. doi: 10.1016/S0092-8674(00)80189-0. PubMed DOI

Tesařová M, Zikmund T, Kaucká M, Adameyko I, Jaroš J, Paloušek D, Škaroupka D, Kaiser J. Use of micro computed-tomography and 3D printing for reverse engineering of mouse embryo nasal capsule. Journal of Instrumentation. 2016;11:C03006. doi: 10.1088/1748-0221/11/03/C03006. DOI

Theis S, Patel K, Valasek P, Otto A, Pu Q, Harel I, Tzahor E, Tajbakhsh S, Christ B, Huang R. The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature. Development. 2010;137:2961–2971. doi: 10.1242/dev.049726. PubMed DOI

Tremblay P, Dietrich S, Mericskay M, Schubert FR, Li Z, Paulin D. A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors. Developmental Biology. 1998;203:49–61. doi: 10.1006/dbio.1998.9041. PubMed DOI

Valasek P, Theis S, Krejci E, Grim M, Maina F, Shwartz Y, Otto A, Huang R, Patel K. Somitic origin of the medial border of the mammalian scapula and its homology to the avian scapula blade. Journal of Anatomy. 2010;216:482–488. doi: 10.1111/j.1469-7580.2009.01200.x. PubMed DOI PMC

Verzi MP, McCulley DJ, De Val S, Dodou E, Black BL. The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Developmental Biology. 2005;287:134–145. doi: 10.1016/j.ydbio.2005.08.041. PubMed DOI

Yabe T, Hoshijima K, Yamamoto T, Takada S. Quadruple zebrafish mutant reveals different roles of Mesp genes in somite segmentation between mouse and zebrafish. Development. 2016;143:2842–2852. doi: 10.1242/dev.133173. PubMed DOI PMC

Yang L, Cai CL, Lin L, Qyang Y, Chung C, Monteiro RM, Mummery CL, Fishman GI, Cogen A, Evans S. Isl1Cre reveals a common Bmp pathway in heart and limb development. Development. 2006;133:1575–1585. doi: 10.1242/dev.02322. PubMed DOI PMC

Yokomizo T, Yamada-Inagawa T, Yzaguirre AD, Chen MJ, Speck NA, Dzierzak E. Whole-mount three-dimensional imaging of internally localized immunostained cells within mouse embryos. Nature Protocols. 2012;7:421–431. doi: 10.1038/nprot.2011.441. PubMed DOI PMC

Zhang Z, Huynh T, Baldini A. Mesodermal expression of Tbx1 is necessary and sufficient for pharyngeal arch and cardiac outflow tract development. Development. 2006;133:3587–3595. doi: 10.1242/dev.02539. PubMed DOI PMC

Ziermann JM, Freitas R, Diogo R. Muscle development in the shark Scyliorhinus canicula: implications for the evolution of the gnathostome head and paired appendage musculature. Frontiers in Zoology. 2017;14:31. doi: 10.1186/s12983-017-0216-y. PubMed DOI PMC

Ziermann JM, Clement AM, Ericsson R, Olsson L. Cephalic muscle development in the Australian lungfish, Neoceratodus forsteri. Journal of Morphology. 2018a;279:494–516. doi: 10.1002/jmor.20784. PubMed DOI

Ziermann JM, Diogo R, Noden DM. Neural crest and the patterning of vertebrate craniofacial muscles. Genesis. 2018b;56:e23097. doi: 10.1002/dvg.23097. PubMed DOI

Zoupa M, Seppala M, Mitsiadis T, Cobourne MT. Tbx1 is expressed at multiple sites of epithelial-mesenchymal interaction during early development of the facial complex. The International Journal of Developmental Biology. 2006;50:504–510. doi: 10.1387/ijdb.052116mz. PubMed DOI

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