Multiple embryonic sources converge to form the pectoral girdle skeleton in zebrafish.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
26 Jul 2024
26 Jul 2024
Historique:
received:
27
07
2023
accepted:
19
07
2024
medline:
27
7
2024
pubmed:
27
7
2024
entrez:
26
7
2024
Statut:
epublish
Résumé
The morphological transformation of the pectoral/shoulder girdle is fundamental to the water-to-land transition in vertebrate evolution. Although previous studies have resolved the embryonic origins of tetrapod shoulder girdles, those of fish pectoral girdles remain uncharacterized, creating a gap in the understanding of girdle transformation mechanisms from fish to tetrapods. Here, we identify the embryonic origins of the zebrafish pectoral girdle, including the cleithrum as an ancestral girdle element lost in extant tetrapods. Our combinatorial approach of photoconversion and genetic lineage tracing demonstrates that cleithrum development combines four adjoining embryonic populations. A comparison of these pectoral girdle progenitors with extinct and extant vertebrates highlights that cleithrum loss, indispensable for neck evolution, is associated with the disappearance of its unique developmental environment at the head/trunk interface. Overall, our study establishes an embryological framework for pectoral/shoulder girdle formation and provides evolutionary trajectories from their origin in water to diversification on land.
Identifiants
pubmed: 39060278
doi: 10.1038/s41467-024-50734-x
pii: 10.1038/s41467-024-50734-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6313Informations de copyright
© 2024. The Author(s).
Références
Goodrich, E. S. Studies on the Structure and Development of Vertebrates (Dover Publications Inc, 1930).
McGonnell, I. M. The evolution of the pectoral girdle. J. Anat. 199, 189–194 (2001).
pubmed: 11523822
pmcid: 1594952
doi: 10.1046/j.1469-7580.2001.19910189.x
Gegenbaur, C. Clavicula und Cleithrum. Morphol. Jahrb. 23, 1–20 (1895).
Matsuoka, T. et al. Neural crest origins of the neck and shoulder. Nature 436, 347–355 (2005).
pubmed: 16034409
pmcid: 1352163
doi: 10.1038/nature03837
Gess, R. & Ahlberg, P. E. A tetrapod fauna from within the Devonian Antarctic circle. Science 360, 1120–1124 (2018).
pubmed: 29880689
doi: 10.1126/science.aaq1645
Jollie, M. Chordate Morphology (Reinhold, 1962).
Romer, A. S. & Parsons, T. S. The Vertebrate Body 6th edn, Vol. 656 (Thomson Learning, 1986).
Lyson, T. R. et al. Homology of the enigmatic nuchal bone reveals novel reorganization of the shoulder girdle in the evolution of the turtle shell. Evol. Dev. 15, 317–325 (2013).
pubmed: 24074278
doi: 10.1111/ede.12041
Romer, A. S. Osteology of the Reptiles Reprint edn (Krieger Publishing Company, 1997).
Nagashima, H. et al. Developmental origin of the clavicle, and its implications for the evolution of the neck and the paired appendages in vertebrates. J. Anat. 229, 536–548 (2016).
pubmed: 27279028
pmcid: 5013064
doi: 10.1111/joa.12502
Heude, E. et al. Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues. eLife 7, e40179 (2018).
pubmed: 30451684
pmcid: 6310459
doi: 10.7554/eLife.40179
Adachi, N., Bilio, M., Baldini, A. & Kelly, R. G. Cardiopharyngeal mesoderm origins of musculoskeletal and connective tissues in the mammalian pharynx. Development 147, dev185256 (2020).
pubmed: 32014863
doi: 10.1242/dev.185256
Nomaru, H. et al. Single cell multi-omic analysis identifies a Tbx1-dependent multilineage primed population in murine cardiopharyngeal mesoderm. Nat. Commun. 12, 6645 (2021).
pubmed: 34789765
pmcid: 8599455
doi: 10.1038/s41467-021-26966-6
Prummel, K. D., Nieuwenhuize, S. & Mosimann, C. The lateral plate mesoderm. Development 147, dev175059 (2020).
Wang, W. et al. A single-cell transcriptional roadmap for cardiopharyngeal fate diversification. Nat. Cell Biol. 21, 674–686 (2019).
pubmed: 31160712
pmcid: 7491489
doi: 10.1038/s41556-019-0336-z
Lescroart, F., Dumas, C. E., Adachi, N. & Kelly, R. G. Emergence of heart and branchiomeric muscles in cardiopharyngeal mesoderm. Exp. Cell Res. 410, 112931 (2022).
pubmed: 34798131
doi: 10.1016/j.yexcr.2021.112931
Shearman, R. M., Tulenko, F. J. & Burke, A. C. 3D reconstructions of quail-chick chimeras provide a new fate map of the avian scapula. Dev. Biol. 355, 1–11 (2011).
pubmed: 21527257
doi: 10.1016/j.ydbio.2011.03.032
Valasek, P. et al. Somitic origin of the medial border of the mammalian scapula and its homology to the avian scapula blade. J. Anat. 216, 482–488 (2010).
pubmed: 20136669
pmcid: 2849525
doi: 10.1111/j.1469-7580.2009.01200.x
Durland, J. L., Sferlazzo, M., Logan, M. & Burke, A. C. Visualizing the lateral somitic frontier in the Prx1Cre transgenic mouse. J. Anat. 212, 590–602 (2008).
pubmed: 18430087
pmcid: 2409079
doi: 10.1111/j.1469-7580.2008.00879.x
Piekarski, N. & Olsson, L. A somitic contribution to the pectoral girdle in the axolotl revealed by long-term fate mapping. Evol. Dev. 13, 47–57 (2011).
pubmed: 21210942
doi: 10.1111/j.1525-142X.2010.00455.x
Fabian, P. & Crump, J. G. Reassessing the embryonic origin and potential of craniofacial ectomesenchyme. Semin. Cell Dev. Biol. 138, 45–53 (2023).
pubmed: 35331627
doi: 10.1016/j.semcdb.2022.03.018
Etchevers, H. C., Dupin, E. & Le Douarin, N. M. The diverse neural crest: from embryology to human pathology. Development 146, dev169821 (2019).
Epperlein, H. H., Khattak, S., Knapp, D., Tanaka, E. M. & Malashichev, Y. B. Neural crest does not contribute to the neck and shoulder in the axolotl (Ambystoma mexicanum). PLoS One 7, e52244 (2012).
pubmed: 23300623
pmcid: 3531446
doi: 10.1371/journal.pone.0052244
McGonnell, I. M., McKay, I. J. & Graham, A. A population of caudally migrating cranial neural crest cells: functional and evolutionary implications. Dev. Biol. 236, 354–363 (2001).
pubmed: 11476577
doi: 10.1006/dbio.2001.0330
Aoto, K. et al. Mef2c-F10N enhancer driven β-galactosidase (LacZ) and Cre recombinase mice facilitate analyses of gene function and lineage fate in neural crest cells. Dev. Biol. 402, 3–16 (2015).
pubmed: 25794678
pmcid: 4433593
doi: 10.1016/j.ydbio.2015.02.022
Masselink, W. et al. A somitic contribution to the apical ectodermal ridge is essential for fin formation. Nature 535, 542–546 (2016).
pubmed: 27437584
doi: 10.1038/nature18953
Kague, E. et al. Skeletogenic fate of zebrafish cranial and trunk neural crest. PLoS ONE 7, e47394 (2012).
pubmed: 23155370
pmcid: 3498280
doi: 10.1371/journal.pone.0047394
Mercader, N. Early steps of paired fin development in zebrafish compared with tetrapod limb development. Dev. Growth Differ. 49, 421–437 (2007).
pubmed: 17587327
doi: 10.1111/j.1440-169X.2007.00942.x
Mongera, A. et al. Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells. Development 140, 916–925 (2013).
pubmed: 23362350
doi: 10.1242/dev.091066
Felker, A. et al. Continuous addition of progenitors forms the cardiac ventricle in zebrafish. Nat. Commun. 9, 2001 (2018).
pubmed: 29784942
pmcid: 5962599
doi: 10.1038/s41467-018-04402-6
Prummel, K. D. et al. Hand2 delineates mesothelium progenitors and is reactivated in mesothelioma. Nat. Commun. 13, 1677 (2022).
pubmed: 35354817
pmcid: 8967825
doi: 10.1038/s41467-022-29311-7
Mao, Q., Stinnett, H. K. & Ho, R. K. Asymmetric cell convergence-driven zebrafish fin bud initiation and pre-pattern requires Tbx5a control of a mesenchymal Fgf signal. Development 142, 4329–4339 (2015).
pubmed: 26525676
pmcid: 4689218
Sagarin, K. A., Redgrave, A. C., Mosimann, C., Burke, A. C. & Devoto, S. H. Anterior trunk muscle shows mix of axial and appendicular developmental patterns. Dev. Dyn. 248, 961–968 (2019).
pubmed: 31386244
pmcid: 6823925
doi: 10.1002/dvdy.95
Minchin, J. E. N. et al. Oesophageal and sternohyal muscle fibres are novel Pax3-dependent migratory somite derivatives essential for ingestion. Development 140, 2972–2984 (2013).
pubmed: 23760954
pmcid: 3699282
doi: 10.1242/dev.090050
Talbot, J. C. et al. Muscle precursor cell movements in zebrafish are dynamic and require Six family genes. Development 146, dev171421 (2019).
pubmed: 31023879
pmcid: 6550023
doi: 10.1242/dev.171421
Hatta, K., Tsujii, H. & Omura, T. Cell tracking using a photoconvertible fluorescent protein. Nat. Protoc. 1, 960–967 (2006).
pubmed: 17406330
doi: 10.1038/nprot.2006.96
Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. & Schilling, T. F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253–310 (1995).
pubmed: 8589427
doi: 10.1002/aja.1002030302
Lee, R. T. H., Knapik, E. W., Thiery, J. P. & Carney, T. J. An exclusively mesodermal origin of fin mesenchyme demonstrates that zebrafish trunk neural crest does not generate ectomesenchyme. Development 140, 2923–2932 (2013).
pubmed: 23739134
pmcid: 3699280
doi: 10.1242/dev.093534
Wardle, F. C. & Papaioannou, V. E. Teasing out T-box targets in early mesoderm. Curr. Opin. Genet. Dev. 18, 418–425 (2008).
pubmed: 18778771
pmcid: 2700021
doi: 10.1016/j.gde.2008.07.017
Mosimann, C. et al. Chamber identity programs drive early functional partitioning of the heart. Nat. Commun. 6, 8146 (2015).
pubmed: 26306682
doi: 10.1038/ncomms9146
Lalonde, R. L. et al. Heterogeneity and genomic loci of ubiquitous transgenic Cre reporter lines in zebrafish. Dev. Dyn. 251, 1754–1773 (2022).
pubmed: 35582941
pmcid: 10069295
doi: 10.1002/dvdy.499
Šestak, M. S., Božičević, V., Bakarić, R., Dunjko, V. & Domazet-Lošo, T. Phylostratigraphic profiles reveal a deep evolutionary history of the vertebrate head sensory systems. Front. Zool. 10, 18 (2013).
pubmed: 23587066
pmcid: 3636138
doi: 10.1186/1742-9994-10-18
McCarroll, M. N. et al. Graded levels of Pax2a and Pax8 regulate cell differentiation during sensory placode formation. Development 139, 2740–2750 (2012).
pubmed: 22745314
pmcid: 3392703
doi: 10.1242/dev.076075
Onimaru, K., Shoguchi, E., Kuratani, S. & Tanaka, M. Development and evolution of the lateral plate mesoderm: Comparative analysis of amphioxus and lamprey with implications for the acquisition of paired fins. Dev. Biol. 359, 124–136 (2011).
pubmed: 21864524
doi: 10.1016/j.ydbio.2011.08.003
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. Zool. Lett. 4, 5 (2018).
doi: 10.1186/s40851-018-0087-x
Arnold, J. S. et al. Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development 133, 977–987 (2006).
pubmed: 16452092
doi: 10.1242/dev.02264
Kuratani, S. & Ahlberg, P. E. Evolution of the vertebrate neurocranium: problems of the premandibular domain and the origin of the trabecula. Zool. Lett. 4, 1 (2018).
doi: 10.1186/s40851-017-0083-6
Gans, C. & Northcutt, R. G. Neural crest and the origin of vertebrates: a new head. Science 220, 268–273 (1983).
pubmed: 17732898
doi: 10.1126/science.220.4594.268
Stundl, J. et al. Migratory patterns and evolutionary plasticity of cranial neural crest cells in ray-finned fishes. Dev. Biol. 467, 14–29 (2020).
pubmed: 32835652
pmcid: 7572781
doi: 10.1016/j.ydbio.2020.08.007
Sato, M. & Yost, H. J. Cardiac neural crest contributes to cardiomyogenesis in zebrafish. Dev. Biol. 257, 127–139 (2003).
pubmed: 12710962
doi: 10.1016/S0012-1606(03)00037-X
Montero-Balaguer, M. et al. The mother superior mutation ablates foxd3 activity in neural crest progenitor cells and depletes neural crest derivatives in zebrafish. Dev. Dyn. 235, 3199–3212 (2006).
pubmed: 17013879
doi: 10.1002/dvdy.20959
Abrial, M. et al. TGF-β signaling is necessary and sufficient for pharyngeal arch artery angioblast formation. Cell Rep. 20, 973–983 (2017).
pubmed: 28746880
pmcid: 5565225
doi: 10.1016/j.celrep.2017.07.002
Kaufman, C. K. et al. A zebrafish melanoma model reveals emergence of neural crest identity during melanoma initiation. Science 351, aad2197 (2016).
pubmed: 26823433
pmcid: 4868069
doi: 10.1126/science.aad2197
Luo, R., An, M., Arduini, B. L. & Henion, P. D. Specific pan-neural crest expression of zebrafish crestin throughout embryonic development. Dev. Dyn. 220, 169–174 (2001).
pubmed: 11169850
doi: 10.1002/1097-0177(2000)9999:9999<::AID-DVDY1097>3.0.CO;2-1
Dutton, J. R. et al. An evolutionarily conserved intronic region controls the spatiotemporal expression of the transcription factor Sox10. BMC Dev. Biol. 8, 105 (2008).
pubmed: 18950534
pmcid: 2601039
doi: 10.1186/1471-213X-8-105
Giovannone, D. et al. Programmed conversion of hypertrophic chondrocytes into osteoblasts and marrow adipocytes within zebrafish bones. eLife 8, e42736 (2019).
pubmed: 30785394
pmcid: 6398980
doi: 10.7554/eLife.42736
Carney, T. J. et al. A direct role for Sox10 in specification of neural crest-derived sensory neurons. Development 133, 4619–4630 (2006).
pubmed: 17065232
doi: 10.1242/dev.02668
Heude, É., Shaikho, S. & Ekker, M. The dlx5a/dlx6a genes play essential roles in the early development of zebrafish median fin and pectoral structures. PLoS ONE 9, e98505 (2014).
pubmed: 24858471
pmcid: 4032342
doi: 10.1371/journal.pone.0098505
Grandel, H. et al. Retinoic acid signalling in the zebrafish embryo is necessary during pre-segmentation stages to pattern the anterior-posterior axis of the CNS and to induce a pectoral fin bud. Development 129, 2851–2865 (2002).
pubmed: 12050134
doi: 10.1242/dev.129.12.2851
Neumann, C. J., Grandel, H., Gaffield, W., Schulte-Merker, S. & Nüsslein-Volhard, C. Transient establishment of anteroposterior polarity in the zebrafish pectoral fin bud in the absence of sonic hedgehog activity. Development 126, 4817–4826 (1999).
pubmed: 10518498
doi: 10.1242/dev.126.21.4817
Trinajstic, K. et al. Fossil musculature of the most primitive jawed vertebrates. Science 341, 160–164 (2013).
pubmed: 23765280
doi: 10.1126/science.1237275
Sleight, V. A. & Gillis, J. A. Embryonic origin and serial homology of gill arches and paired fins in the skate, Leucoraja erinacea. eLife 9, e60635 (2020).
pubmed: 33198887
pmcid: 7671686
doi: 10.7554/eLife.60635
Evans, D. J. & Noden, D. M. Spatial relations between avian craniofacial neural crest and paraxial mesoderm cells. Dev. Dyn. 235, 1310–1325 (2006).
pubmed: 16395689
doi: 10.1002/dvdy.20663
Tabler, J. M. et al. Cilia-mediated Hedgehog signaling controls form and function in the mammalian larynx. eLife 6, e19153 (2017).
pubmed: 28177282
pmcid: 5358977
doi: 10.7554/eLife.19153
Sefton, E. M., Piekarski, N. & Hanken, J. Dual embryonic origin and patterning of the pharyngeal skeleton in the axolotl (Ambystoma mexicanum). Evol. Dev. 17, 175–184 (2015).
pubmed: 25963195
doi: 10.1111/ede.12124
Fischer, S., Draper, B. W. & Neumann, C. J. The zebrafish fgf24 mutant identifies an additional level of Fgf signaling involved in vertebrate forelimb initiation. Development 130, 3515–3524 (2003).
pubmed: 12810598
doi: 10.1242/dev.00537
Wei, J. et al. Distinct ossification trade-offs illuminate the shoulder girdle reconfiguration at the water-to-land transition. bioRxiv https://doi.org/10.1101/2023.07.17.547998 (2023).
Kuratani, S. Spatial distribution of postotic crest cells defines the head/trunk interface of the vertebrate body: embryological interpretation of peripheral nerve morphology and evolution of the vertebrate head. Anat. Embryol. 195, 1–13 (1997).
doi: 10.1007/s004290050020
Higashiyama, H. et al. On the vagal cardiac nerves, with special reference to the early evolution of the head-trunk interface. J. Morphol. 277, 1146–1158 (2016).
pubmed: 27216138
doi: 10.1002/jmor.20563
Hirasawa, T. et al. Development of the pectoral lobed fin in the Australian lungfish Neoceratodus forsteri. Front. Ecol. Evol. https://doi.org/10.3389/fevo.2021.679633 (2021).
Greil, A. Entwickelungsgeschichte des Kopfes und des Blutgefäßsystems von Ceratodus forsteri. II. Die epigenetischen Erwerbungen während der Stadien 39-48. Denkschriften der Medicinisch-Naturwissenschaftlichen Ges. zu Jena. 4, 935–1492 (1913).
Trinajstic, K. et al. Exceptional preservation of organs in Devonian placoderms from the Gogo lagerstätte. Science 377, 1311–1314 (2022).
pubmed: 36107996
doi: 10.1126/science.abf3289
Janvier, P., Percy, L. R. & Potter, I. C. The arrangement of the heart chambers and associated blood vessels in the Devonian osteostracan Norselaspis glacialis. A reinterpretation based on recent studies of the circulatory system in lampreys. J. Zool. 223, 567–576 (1991).
doi: 10.1111/j.1469-7998.1991.tb04388.x
Adachi, N., Robinson, M., Goolsbee, A. & Shubin, N. H. Regulatory evolution of Tbx5 and the origin of paired appendages. Proc. Natl Acad. Sci. USA 113, 10115–10120 (2016).
pubmed: 27503876
pmcid: 5018757
doi: 10.1073/pnas.1609997113
Janvier, P. Early Vertebrates (Oxford University Press, 1996).
Brazeau, M. D. et al. Fossil evidence for a pharyngeal origin of the vertebrate pectoral girdle. Nature 623, 550–554 (2023).
pubmed: 37914937
pmcid: 10651482
doi: 10.1038/s41586-023-06702-4
Gegenbaur, C. Zur Morphologie der Gliedmaassen der Wirbeltiere. Morpho. Jahrb. 2, 396–420 (1876).
Thacher, J. K. Median and paired fins: a contribution to the history of vertebrate limbs. Trans. Conn. Acad. Arts Sci. 3, 281–308 (1877).
Balfour, F. M. On the development of the skeleton of the paired fins of Elasmobranchii, considered in relation to its bearings on the nature of the limbs of the Vertebrata. Proc. Zool. Soc. Lond. 49, 656–670 (1881).
doi: 10.1111/j.1096-3642.1881.tb01323.x
Williston, S. W. The Osteology of the Reptiles, reprint edn (Krieger Publishing Company, 1925).
MacDougall, M. J. & Modesto, S. P. & Botha-Brink, J. The postcranial skeleton of the Early Triassic parareptile Sauropareion anoplus, with a discussion of possible life history. Acta Palaeontol. Polonica 58, 737–749 (2013).
Hirasawa, T. & Kuratani, S. A new scenario of the evolutionary derivation of the mammalian diaphragm from shoulder muscles. J. Anat. 222, 504–517 (2013).
pubmed: 23448284
pmcid: 3633340
doi: 10.1111/joa.12037
Müller, J. et al. Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. Proc. Natl Acad. Sci. USA 107, 2118–2123 (2010).
pubmed: 20080660
pmcid: 2836685
doi: 10.1073/pnas.0912622107
Lours, C. & Dietrich, S. The dissociation of the Fgf-feedback loop controls the limbless state of the neck. Development 132, 5553–5564 (2005).
pubmed: 16314488
doi: 10.1242/dev.02164
Hirasawa, T., Fujimoto, S. & Kuratani, S. Expansion of the neck reconstituted the shoulder-diaphragm in amniote evolution. Dev., Growth Differ. 58, 143–153 (2016).
pubmed: 26510533
doi: 10.1111/dgd.12243
Sefton, E. M., Gallardo, M. & Kardon, G. Developmental origin and morphogenesis of the diaphragm, an essential mammalian muscle. Dev. Biol. 440, 64–73 (2018).
pubmed: 29679560
pmcid: 6089379
doi: 10.1016/j.ydbio.2018.04.010
Sefton, E. M. et al. Fibroblast-derived Hgf controls recruitment and expansion of muscle during morphogenesis of the mammalian diaphragm. eLife 11, e74592 (2022).
pubmed: 36154712
pmcid: 9514848
doi: 10.7554/eLife.74592
Schneider, R. A. Neural crest can form cartilages normally derived from mesoderm during development of the avian head skeleton. Dev. Biol. 208, 441–455 (1999).
pubmed: 10191057
doi: 10.1006/dbio.1999.9213
Teng, C. S., Cavin, L., Maxson, R. E. J., Sánchez-Villagra, M. R. & Crump, J. G. Resolving homology in the face of shifting germ layer origins: Lessons from a major skull vault boundary. eLife 8, e52814 (2019).
pubmed: 31869306
pmcid: 6927740
doi: 10.7554/eLife.52814
Hamilton, F. An Account of the Fishes Found in the River Ganges and its Branches Vol. 415 (Isha Books, 1822).
Mosimann, C. et al. Ubiquitous transgene expression and cre-based recombination driven by the ubiquitin promoter in zebrafish. Development 138, 169–177 (2011).
pubmed: 21138979
pmcid: 2998170
doi: 10.1242/dev.059345
Choi, H. M. T. et al. Third-generation in situ hybridization chain reaction: multiplexed, quantitative, sensitive, versatile, robust. Development 145, dev165753 (2018).
pubmed: 29945988
pmcid: 6031405
doi: 10.1242/dev.165753
Ibarra-García-Padilla, R., Howard, A. G. A., Singleton, E. W. & Uribe, R. A. A protocol for whole-mount immuno-coupled hybridization chain reaction (WICHCR) in zebrafish embryos and larvae. STAR Protoc. 2, 100709 (2021).
pubmed: 34401776
pmcid: 8348268
doi: 10.1016/j.xpro.2021.100709
Hu, Y., Limaye, A. & Lu, J. Three-dimensional segmentation of computed tomography data using drishti paint: new tools and developments. R. Soc. Open Sci. 7, 201033 (2020).
pubmed: 33489265
pmcid: 7813226
doi: 10.1098/rsos.201033
Hildebrand, D. G. C. et al. Whole-brain serial-section electron microscopy in larval zebrafish. Nature 545, 345–349 (2017).
pubmed: 28489821
pmcid: 5594570
doi: 10.1038/nature22356