A median fin derived from the lateral plate mesoderm and the origin of paired fins.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
Jun 2023
Historique:
received: 05 08 2022
accepted: 19 04 2023
medline: 16 6 2023
pubmed: 25 5 2023
entrez: 24 5 2023
Statut: ppublish

Résumé

The development of paired appendages was a key innovation during evolution and facilitated the aquatic to terrestrial transition of vertebrates. Largely derived from the lateral plate mesoderm (LPM), one hypothesis for the evolution of paired fins invokes derivation from unpaired median fins via a pair of lateral fin folds located between pectoral and pelvic fin territories

Identifiants

pubmed: 37225983
doi: 10.1038/s41586-023-06100-w
pii: 10.1038/s41586-023-06100-w
pmc: PMC10266977
doi:

Substances chimiques

Bone Morphogenetic Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

543-549

Subventions

Organisme : NHLBI NIH HHS
ID : F31 HL167580
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM141742
Pays : United States

Informations de copyright

© 2023. The Author(s).

Références

Coates, M. I. The evolution of paired fins. Theory Biosci. 122, 266–287 (2003).
doi: 10.1007/s12064-003-0057-4
Freitas, R., Zhang, G. & Cohn, M. J. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442, 1033–1037 (2006).
pubmed: 16878142 doi: 10.1038/nature04984
Gegenbaur, C. Elements of Comparative Anatomy (Macmillan and Company, 1878).
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
Mivart, S. G. Notes on the fins of elasmobranchs, with considerations on the nature and homologues of vertebrate limbs. Trans. Zool. Soc. Lond. 10, 439–484 (1879).
doi: 10.1111/j.1096-3642.1879.tb00460.x
Gillis, J. A., Dahn, R. D. & Shubin, N. H. Shared developmental mechanisms pattern the vertebrate gill arch and paired fin skeletons. Proc. Natl Acad. Sci. USA 106, 5720–5724 (2009).
pubmed: 19321424 pmcid: 2667079 doi: 10.1073/pnas.0810959106
Diogo, R. Cranial or postcranial—dual origin of the pectoral appendage of vertebrates combining the fin-fold and gill-arch theories? Dev. Dyn. 249, 1182–1200 (2020).
pubmed: 32395826 doi: 10.1002/dvdy.192
Bemis, W. E. & Grande, L. in Mesozoic Fishes 2: Systematics and Fossil Record. (eds Arratia, G. & Schultze, H.-P.) 41–68 Vrelag Dr. F. Pfeil, 1999).
Zhang, X. G. & Hou, X. G. Evidence for a single median fin-fold and tail in the Lower Cambrian vertebrate, Haikouichthys ercaicunensis. J. Evol. Biol. 17, 1162–1166 (2004).
pubmed: 15312089 doi: 10.1111/j.1420-9101.2004.00741.x
Shu, D. G. et al. Lower Cambrian vertebrates from south China. Nature 402, 42–46 (1999).
doi: 10.1038/46965
Wilson, M. V. H., Hanke, G. F. & Märss, T. in Major Transitions in Vertebrate Evolution (eds Anderson, J. & Sues, H.-D.) Ch. 3, 122–149 (Indiana Univ. Press, 2007).
Sansom, R. S., Freedman, K. I. M., Gabbott, S. E., Aldridge, R. J. & Purnell, M. A. Taphonomy and affinity of an enigmatic Silurian vertebrate, Jamoytius kerwoodi White. Palaeontology 53, 1393–1409 (2010).
doi: 10.1111/j.1475-4983.2010.01019.x
Sansom, R. S., Gabbott, S. E. & Purnell, M. A. Unusual anal fin in a Devonian jawless vertebrate reveals complex origins of paired appendages. Biol. Lett. 9, 20130002 (2013).
pubmed: 23576777 pmcid: 3645028 doi: 10.1098/rsbl.2013.0002
Lee, R. T., Thiery, J. P. & Carney, T. J. Dermal fin rays and scales derive from mesoderm, not neural crest. Curr. Biol. 23, R336–R337 (2013).
pubmed: 23660348 doi: 10.1016/j.cub.2013.02.055
Taniguchi, Y. et al. Mesodermal origin of median fin mesenchyme and tail muscle in amphibian larvae. Sci. Rep. 5, 11428 (2015).
pubmed: 26086331 pmcid: 4471895 doi: 10.1038/srep11428
Parichy, D. M., Elizondo, M. R., Mills, M. G., Gordon, T. N. & Engeszer, R. E. Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Dev. Dyn. 238, 2975–3015 (2009).
pubmed: 19891001 pmcid: 3030279 doi: 10.1002/dvdy.22113
Shimada, A. et al. Trunk exoskeleton in teleosts is mesodermal in origin. Nat. Commun. 4, 1639 (2013).
pubmed: 23535660 doi: 10.1038/ncomms2643
Lee, R. T., 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
Okuda, K. S. et al. A zebrafish model of inflammatory lymphangiogenesis. Biol. Open 4, 1270–1280 (2015).
pubmed: 26369931 pmcid: 4610225 doi: 10.1242/bio.013540
Asharani, P. V. et al. Attenuated BMP1 function compromises osteogenesis, leading to bone fragility in humans and zebrafish. Am. J. Hum. Genet. 90, 661–674 (2012).
pubmed: 22482805 pmcid: 3322236 doi: 10.1016/j.ajhg.2012.02.026
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
Yelon, D. et al. The bHLH transcription factor hand2 plays parallel roles in zebrafish heart and pectoral fin development. Development 127, 2573–2582 (2000).
pubmed: 10821756 doi: 10.1242/dev.127.12.2573
Yin, C., Kikuchi, K., Hochgreb, T., Poss, K. D. & Stainier, D. Y. R. Hand2 regulates extracellular matrix remodeling essential for gut-looping morphogenesis in zebrafish. Dev. Cell 18, 973–984 (2010).
pubmed: 20627079 pmcid: 2908152 doi: 10.1016/j.devcel.2010.05.009
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
Richardson, M. K. & Wright, G. M. Developmental transformations in a normal series of embryos of the sea lamprey Petromyzon marinus (Linnaeus). J. Morphol. 257, 348–363 (2003).
pubmed: 12833373 doi: 10.1002/jmor.10119
Kemp, A. Rearing of embryos and larvae of the Australian Lungfish, Neoceratodus forsteri, under laboratory conditions. Copeia 1981, 776–784 (1981).
doi: 10.2307/1444177
Nieuwkoop, P. D. & Faber, J. Normal Table of Xenopus laevis (Daudin): A Systematical and Chronological Survey of the Development from the Fertilized Egg till the End of Metamorphosis 1 edn (Garland Publishing, 1994).
Hammerschmidt, M. et al. dino and mercedes, two genes regulating dorsal development in the zebrafish embryo. Development 123, 95–102 (1996).
pubmed: 9007232 doi: 10.1242/dev.123.1.95
Kon, T. et al. The genetic basis of morphological diversity in domesticated goldfish. Curr. Biol. 30, 2260–2274.e6 (2020).
pubmed: 32392470 doi: 10.1016/j.cub.2020.04.034
Abe, G. et al. The origin of the bifurcated axial skeletal system in the twin-tail goldfish. Nat. Commun. 5, 3360 (2014).
pubmed: 24569511 doi: 10.1038/ncomms4360
Watase, S. On the caudal and anal fins of goldfishes. J. Sci. Coll. Imp. Univ. Tokyo 1, 247–267 (1887).
Yonei-Tamura, S. et al. Competent stripes for diverse positions of limbs/fins in gnathostome embryos. Evol. Dev. 10, 737–745 (2008).
pubmed: 19021745 doi: 10.1111/j.1525-142X.2008.00288.x
Smith, B. G. in The Bashford Dean Memorial Volume: Archaic Fishes Vol. 2 (ed. E. W. Gudger) Article VI, 333–506 (The American Museum of Natural History, 1937)
Cole, F. J. A monograph on the general morphology of the myxinoid fishes, based on a study of Myxine Part 1. The anatomy of the skeleton. Trans. R. Soc. Edinb. 41, 749–788 (1905).
doi: 10.1017/S0080456800035572
Larouche, O., Zelditch, M. L. & Cloutier, R. A critical appraisal of appendage disparity and homology in fishes. Fish Fish. 20, 1138–1175 (2019).
doi: 10.1111/faf.12402
Blom, H. New birkeniid anaspid from the Lower Devonian of Scotland and its phylogenetic implications. Palaeontology 55, 641–652 (2012).
doi: 10.1111/j.1475-4983.2012.01142.x
Kragl, M. et al. Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 460, 60–65 (2009).
pubmed: 19571878 doi: 10.1038/nature08152
Richardson, L. R. Neomyxine n.g. (Cyclostomata) based on Myxine biniplicata Richardson and Jowett 1951, and further data on the species. Trans. R. Soc. N. Z. 81, 379–383 (1953).
Donoghue, P. C., Forey, P. L. & Aldridge, R. J. Conodont affinity and chordate phylogeny. Biol. Rev. Camb. Philos. Soc. 75, 191–251 (2000).
pubmed: 10881388 doi: 10.1017/S0006323199005472
Janvier, P. & Arsenault, M. The anatomy of Euphanerops longaevus Woodward, 1900, an anaspid-like jawless vertebrate from the Upper Devonian of Miguasha, Quebec, Canada. Geodiversitas 29, 143–216 (2007).
Blom, H. A new anaspid fish from the Middle Silurian Cowie Harbour fish bed of Stonehaven, Scotland. J. Vert. Paleontol. 28, 594–600 (2008).
doi: 10.1671/0272-4634(2008)28[594:ANAFFT]2.0.CO;2
Gai, Z. et al. Galeaspid anatomy and the origin of vertebrate paired appendages. Nature 609, 959–963 (2022).
pubmed: 36171376 doi: 10.1038/s41586-022-04897-6
Ritchie, A. The late Silurian anaspid genus Rhyncholepis from Oesel, Estonia, and Ringerike, Norway. Am. Mus. Novit. 2699, 1–18 (1980).
Mansfield, J. H. & Holland, N. D. Amphioxus tails: source and fate of larval fin rays and the metamorphic transition from an ectodermal to a predominantly mesodermal tail. Acta Zool. 96, 117–125 (2015).
doi: 10.1111/azo.12058
Tulenko, F. J. et al. Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins. Proc. Natl Acad. Sci. USA 110, 11899–11904 (2013).
pubmed: 23818600 pmcid: 3718130 doi: 10.1073/pnas.1304210110
Nuño de la Rosa, L., Müller, G. B. & Metscher, B. D. The lateral mesodermal divide: an epigenetic model of the origin of paired fins. Evol. Dev. 16, 38–48 (2014).
pubmed: 24393466 doi: 10.1111/ede.12061
Iwamatsu, T. Stages of normal development in the medaka Oryzias latipes. Mech. Dev. 121, 605–618 (2004).
pubmed: 15210170 doi: 10.1016/j.mod.2004.03.012
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
Li, I. J., Lee, S. H., Abe, G. & Ota, K. G. Embryonic and postembryonic development of the ornamental twin-tail goldfish. Dev. Dyn. 248, 251–283 (2019).
pubmed: 30687996 pmcid: 6593469 doi: 10.1002/dvdy.15
Tahara, Y. Normal stages of development in the lamprey, Lampetra reissneri (Dybowski). Zool. Sci. 5, 109–118 (1988).
Ballard, W. W., Mellinger, J. & Lechenault, H. A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae). J. Exp. Zool. 267, 318–336 (1993).
doi: 10.1002/jez.1402670309
Okuda, K. S. et al. lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish. Development 139, 2381–2391 (2012).
pubmed: 22627281 pmcid: 4074227 doi: 10.1242/dev.077701
Kwan, K. M. et al. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088–3099 (2007).
pubmed: 17937395 doi: 10.1002/dvdy.21343
Thermes, V. et al. I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech. Dev. 118, 91–98 (2002).
pubmed: 12351173 doi: 10.1016/S0925-4773(02)00218-6
Thisse, C. & Thisse, B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 3, 59–69 (2008).
pubmed: 18193022 doi: 10.1038/nprot.2007.514
Feitosa, N. M. et al. Hemicentin 2 and Fibulin 1 are required for epidermal-dermal junction formation and fin mesenchymal cell migration during zebrafish development. Dev. Biol. 369, 235–248 (2012).
pubmed: 22771579 pmcid: 3423513 doi: 10.1016/j.ydbio.2012.06.023
Ablooglu, A. J., Kang, J., Handin, R. I., Traver, D. & Shattil, S. J. The zebrafish vitronectin receptor: characterization of integrin alphaV and beta3 expression patterns in early vertebrate development. Dev. Dyn. 236, 2268–2276 (2007).
pubmed: 17626277 doi: 10.1002/dvdy.21229
Kaneko, H., Nakatani, Y., Fujimura, K. & Tanaka, M. Development of the lateral plate mesoderm in medaka Oryzias latipes and Nile tilapia Oreochromis niloticus: insight into the diversification of pelvic fin position. J. Anat. 225, 659–674 (2014).
pubmed: 25345789 pmcid: 4262350 doi: 10.1111/joa.12244
Davis, M. C., Dahn, R. D. & Shubin, N. H. An autopodial-like pattern of Hox expression in the fins of a basal actinopterygian fish. Nature 447, 473–476 (2007).
pubmed: 17522683 doi: 10.1038/nature05838
Lea, R., Bonev, B., Dubaissi, E., Vize, P. D. & Papalopulu, N. Multicolor fluorescent in situ mRNA hybridization (FISH) on whole mounts and sections. Methods Mol. Biol. 917, 431–444 (2012).
pubmed: 22956102 doi: 10.1007/978-1-61779-992-1_24
Lea, R., Papalopulu, N., Amaya, E. & Dorey, K. Temporal and spatial expression of FGF ligands and receptors during Xenopus development. Dev. Dyn. 238, 1467–1479 (2009).
pubmed: 19322767 pmcid: 3737481 doi: 10.1002/dvdy.21913
Gilchrist, M. J. et al. Defining a large set of full-length clones from a Xenopus tropicalis EST project. Dev. Biol. 271, 498–516 (2004).
pubmed: 15223350 doi: 10.1016/j.ydbio.2004.04.023
Cerny, R. et al. Evidence for the prepattern/cooption model of vertebrate jaw evolution. Proc. Natl Acad. Sci. USA 107, 17262–17267 (2010).
pubmed: 20855630 pmcid: 2951391 doi: 10.1073/pnas.1009304107
Kemp, H. A., Carmany-Rampey, A. & Moens, C. Generating chimeric zebrafish embryos by transplantation. J. Vis. Exp. 29, 1394 (2009).
Metscher, B. D. MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiol. 9, 11 (2009).
pubmed: 19545439 pmcid: 2717911 doi: 10.1186/1472-6793-9-11

Auteurs

Keh-Weei Tzung (KW)

Institute of Molecular and Cell Biology, A*STAR, Singapore, Singapore.
Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore.

Robert L Lalonde (RL)

Department of Pediatrics, Section of Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, CO, USA.

Karin D Prummel (KD)

Department of Pediatrics, Section of Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, CO, USA.
Department of Molecular Life Sciences, University of Zurich, Zurich, Switzerland.

Harsha Mahabaleshwar (H)

Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore.

Hannah R Moran (HR)

Department of Pediatrics, Section of Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, CO, USA.

Jan Stundl (J)

Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA.
Faculty of Fisheries and Protection of Waters, University of South Bohemia in Ceske Budejovice, Vodnany, Czech Republic.

Amanda N Cass (AN)

Biology Department, Wesleyan University, Middletown, CT, USA.

Yao Le (Y)

Department of Biological Sciences, Faculty of Science, National University of Singapore, Singapore, Singapore.

Robert Lea (R)

Division of Developmental Biology and Medicine, School of Medical Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.

Karel Dorey (K)

Division of Developmental Biology and Medicine, School of Medical Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.

Monika J Tomecka (MJ)

Institute of Molecular and Cell Biology, A*STAR, Singapore, Singapore.

Changqing Zhang (C)

Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore.

Eline C Brombacher (EC)

Department of Molecular Life Sciences, University of Zurich, Zurich, Switzerland.

William T White (WT)

CSIRO National Research Collections Australia, Australia National Fish Collection, Hobart, Tasmania, Australia.

Henry H Roehl (HH)

School of Biosciences, University of Sheffield, Sheffield, UK.

Frank J Tulenko (FJ)

Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia.

Christoph Winkler (C)

Department of Biological Sciences, Faculty of Science, National University of Singapore, Singapore, Singapore.

Peter D Currie (PD)

Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia.
EMBL Australia, Victorian Node, Monash University, Clayton, Victoria, Australia.

Enrique Amaya (E)

Division of Cell Matrix Biology and Regenerative Medicine, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.

Marcus C Davis (MC)

Department of Physical and Biological Sciences, Western New England University, Springfield, MA, USA.

Marianne E Bronner (ME)

Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA.

Christian Mosimann (C)

Department of Pediatrics, Section of Developmental Biology, University of Colorado Anschutz Medical Campus, Aurora, CO, USA. christian.mosimann@cuanschutz.edu.
Department of Molecular Life Sciences, University of Zurich, Zurich, Switzerland. christian.mosimann@cuanschutz.edu.

Tom J Carney (TJ)

Institute of Molecular and Cell Biology, A*STAR, Singapore, Singapore. tcarney@ntu.edu.sg.
Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore. tcarney@ntu.edu.sg.

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