Bone is an evolutionary novelty of vertebrates, likely to have first emerged as part of ancestral dermal armor that consisted of osteogenic and odontogenic components. Whether these early vertebrate structures arose from mesoderm or neural crest cells has been a matter of considerable debate. To examine the developmental origin of the bony part of the dermal armor, we have performed in vivo lineage tracing in the sterlet sturgeon, a representative of nonteleost ray-finned fish that has retained an extensive postcranial dermal skeleton. The results definitively show that sterlet trunk neural crest cells give rise to osteoblasts of the scutes. Transcriptional profiling further reveals neural crest gene signature in sterlet scutes as well as bichir scales. Finally, histological and microCT analyses of ray-finned fish dermal armor show that their scales and scutes are formed by bone, dentin, and hypermineralized covering tissues, in various combinations, that resemble those of the first armored vertebrates. Taken together, our results support a primitive skeletogenic role for the neural crest along the entire body axis, that was later progressively restricted to the cranial region during vertebrate evolution. Thus, the neural crest was a crucial evolutionary innovation driving the origin and diversification of dermal armor along the entire body axis.

Department of Evolutionary Biology Theoretical Biology Unit University of Vienna 1010 Vienna Austria

Department of Integrative Biology Michigan State University East Lansing MI 48824

Department of Organismal Biology Uppsala University SE 75236 Uppsala Sweden

Department of Zoology Faculty of Science Charles University Prague 128 00 Prague Czech Republic

Division of Biology and Biological Engineering California Institute of Technology Pasadena CA 91125

Ecology Evolution and Behavior Program Michigan State University East Lansing MI 48824

Faculty of Fisheries and Protection of Waters University of South Bohemia in Ceske Budejovice 38925 Vodnany Czech Republic

Komentář v

Proc Natl Acad Sci U S A. 2023 Aug 15;120(33):e2310552120. doi: 10.1073/pnas.2310552120. PubMed

Zobrazit více v PubMed

Le Douarin N. M., The Neural Crest (Cambridge University Press, 1982).

Gans C., Northcutt R. G., Neural crest and the origin of vertebrates: A new head. Science 220, 268–274 (1983). PubMed

Hall B. K., The Neural Crest and Neural Crest Cells in Vertebrate Development and Evolution (Springer, US, 2009).

Simoes-Costa M., Bronner M. E., Reprogramming of avian neural crest axial identity and cell fate. Science 352, 1570–1573 (2016). PubMed PMC

McGonnell I. M., Graham A., Trunk neural crest has skeletogenic potential. Curr. Biol. 12, 767–771 (2002). PubMed

Lumsden A. G., Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 103, 155–169 (1988). PubMed

Soldatov R., et al. , Spatiotemporal structure of cell fate decisions in murine neural crest. Science 364, eaas9636 (2019). PubMed

Sire J.-Y., Donoghue P. C. J., Vickaryous M. K., Origin and evolution of the integumentary skeleton in non-tetrapod vertebrates. J. Anat. 214, 409–440 (2009). PubMed PMC

Rocha M., et al. , From head to tail: Regionalization of the neural crest. Development 147, dev193888 (2020). PubMed PMC

Smith M. M., Hall B. K., A developmental model for evolution of the vertebrate exoskeleton and teeth in Evolutionary Biology, Hecht M. K., Maclntyre R. J., Clegg M. T., Eds. (Springer US, 1993), vol. 27, pp. 387–448.

Vickaryous M. K., Sire J.-Y., The integumentary skeleton of tetrapods: Origin, evolution, and development. J. Anat. 214, 441–464 (2009). PubMed PMC

Martik M. L., et al. , Evolution of the new head by gradual acquisition of neural crest regulatory circuits. Nature 574, 675–678 (2019). PubMed PMC

Gillis J. A., Alsema E. C., Criswell K. E., Trunk neural crest origin of dermal denticles in a cartilaginous fish. Proc. Natl. Acad. Sci. U.S.A. 114, 13200–13205 (2017). PubMed PMC

Jing J., et al. , Spatiotemporal single-cell regulatory atlas reveals neural crest lineage diversification and cellular function during tooth morphogenesis. Nat. Commun. 13, 4803 (2022). PubMed PMC

Smith M. M., Hall B. K., Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol. Rev. 65, 277–373 (1990). PubMed

Keating J. N., Marquart C. L., Donoghue P. C., Histology of the heterostracan dermal skeleton: Insight into the origin of the vertebrate mineralised skeleton. J. Morphol. 276, 657–680 (2015). PubMed PMC

Shimada A., et al. , Trunk exoskeleton in teleosts is mesodermal in origin. Nat. Commun. 4, 1638–1639 (2013). PubMed PMC

Mongera A., Nüsslein-Volhard C., Scales of fish arise from mesoderm. Curr. Biol. 23, R338–R339 (2013). PubMed

Lee R. T. H., Thiery J. P., Carney T. J., Dermal fin rays and scales derive from mesoderm, not neural crest. Curr. Biol. 23, R336–R337 (2013). PubMed

Smith M., et al. , Trunk neural crest origin of caudal fin mesenchyme in the zebrafish Brachydanio rerio. Proc. Biol. Sci. 256, 137–145 (1994).

Kague E., et al. , Skeletogenic fate of zebrafish cranial and trunk neural crest. PLoS One 7, 1–13 (2012). PubMed PMC

Hilton E. J., Grande L., Review of the fossil record of sturgeons, family Acipenseridae (Actinopterygii: Acipenseriformes), from North America. J. Paleontol. 80, 672–680 (2006).

Alison M., et al. , Paddlefish and sturgeon (Chondrostei: Acipenseriformes: Polyodontidae and Acipenseridae) from lower Paleocene deposits of Montana, U.S.A. J. Vertebr. Paleontol. 40, 2 (2020).

Sewertzoff A. N., The development of the scales of Acipenser ruthenus. J. Morphol. 42, 523–560 (1926).

Bemis W. E., Findeis E. K., Grande L., An overview of Acipenseriformes. Environ. Biol. Fishes 48, 25–71 (1997).

Qu Q., et al. , New genomic and fossil data illuminate the origin of enamel. Nature 526, 108–111 (2015). PubMed

Hertwig O., Ueber das Hautskelet der Fische. 2: Das Hautskelet der Ganoiden (Lepidosteus und Polypterus). Morphol. Jahrb. 5, 1–21 (1879).

Kerr T., The scales of primitive living actinopterygians. Proc. Zool. Soc. Lond. 122, 55–78 (1952).

Sire J.-Y., Scales in young Polypterus senegalus are elasmoid: new phylogenetic implications. Am. J. Anat. 186, 315–323 (1989). PubMed

Sire J.-Y., Light and TEM study of nonregenerated and experimentally regenerated scales of Lepisosteus oculatus (Holostei) with particular attention to ganoine formation. Anat. Rec. 240, 189–207 (1994). PubMed

Mori S., Nakamura T., Redeployment of odontode gene regulatory network underlies dermal denticle formation and evolution in suckermouth armored catfish. Sci. Rep. 12, 6172 (2022). PubMed PMC

Liu Z., et al. , The channel catfish genome sequence provides insights into the evolution of scale formation in teleosts. Nat. Commun. 7, 11757 (2016). PubMed PMC

Rivera-Rivera C. J., Montoya-Burgos J. I., Trunk dental tissue evolved independently from underlying dermal bony plates but is associated with surface bones in living odontode-bearing catfish. Proc. Biol. Sci. 284, 20171831 (2017). PubMed PMC

Martik M. L., Bronner M. E., Regulatory logic underlying diversification of the neural crest. Trends Genet. 33, 715–727 (2017). PubMed PMC

Smith M. M., Putative skeletal neural crest cells in early late ordovician vertebrates from colorado. Science 251, 301–303 (1991). PubMed

Repetski J. E., A fish from the Upper Cambrian of North America. Science 200, 529–531 (1978). PubMed

Smith M. P., Sansom I. J., Repetski E. J., Histology of the first fish. Science 380, 702–704 (1996).

Giles S., Rücklin M., Donoghue P. C. J., Histology of ‘placoderm’ dermal skeletons: Implications for the nature of the ancestral gnathostome. J. Morphol. 274, 627–644 (2013). PubMed PMC

Keating J. N., Donoghue P. C. J., Histology and affinity of anaspids, and the early evolution of the vertebrate dermal skeleton. Proc. Biol. Sci. 283, 20152917 (2016). PubMed PMC

Janvier P., Facts and fancies about early fossil chordates and vertebrates. Nature 520, 483–489 (2015). PubMed

Miyashita T., et al. , Hagfish from the Cretaceous Tethys Sea and a reconciliation of the morphological-molecular conflict in early vertebrate phylogeny. Proc. Natl. Acad. Sci. U.S.A. 116, 2146–2151 (2019). PubMed PMC

Miyashita T., et al. , Non-ammocoete larvae of Paleozoic stem lampreys. Nature 591, 408–412 (2021). PubMed

Chai Y., et al. , Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127, 1671–1679 (2000). PubMed

Matsuoka T., et al. , Neural crest origins of the neck and shoulder. Nature 436, 347–355 (2005). PubMed PMC

Cebra-Thomas J. A., et al. , Evidence that a late-emerging population of trunk neural crest cells forms the plastron bones in the turtle Trachemys scripta. Evol. Dev. 9, 267–277 (2007). PubMed

Cebra-Thomas J. A., et al. , Late-emigrating trunk neural crest cells in turtle embryos generate an osteogenic ectomesenchyme in the plastron. Dev. Dyn. 242, 1223–1235 (2013). PubMed

Krmpotic C. M., et al. , The dorsal integument of the Southern Long-nosed armadillo Dasypus hybridus (Cingulata, Xenarthra), and a possible neural crest origin of the osteoderms. Discussing evolutive consequences for Amniota. J. Mamm. Evol. 28, 635–645 (2021).

Teng C. S., et al. , Resolving homology in the face of shifting germ layer origins: Lessons from a major skull vault boundary. eLife 8, e52814 (2019). PubMed PMC

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 PMC

Sire J.-Y., Akimenko M.-A., Scale development in fish: A review, with description of sonic hedgehog (shh) expression in the zebrafish (Danio rerio). Int. J. Dev. Biol. 48, 233–247 (2004). PubMed

Adameyko I., Elaboration of fates in neural crest lineage during evolution in Evolving Neural Crest Cells, Eames B. F., Medeiros D., Adameyko I., Eds. (CRC Press, Boca Raton, 2020), pp. 157–183

Dettlaff T. A., Ginsburg A. S., Schmalhausen O. I., Sturgeon Fishes: Developmental Biology and Aquaculture (Springer Verlag, 1993).

Choi H. M. T., et al. , Third-generation in situ hybridization chain reaction: Multiplexed, quantitative, sensitive, versatile, robust. Development 145, 1–10 (2018). PubMed PMC

Criswell K. E., Gillis A. J., Resegmentation is an ancestral feature of the gnathostome vertebral skeleton. eLife 9, e51696 (2020). PubMed PMC

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 PMC

Karolchik D., et al. , The UCSC genome browser database. Nucleic Acids Res. 31, 51–54 (2003). PubMed PMC

Langmead B., Salzburg S., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012). PubMed PMC

Liao Y., Smyth G. K., Shi W., featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014). PubMed

Love M. I., Huber W., Anders S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014). PubMed PMC

Gu Z., Eils R., Schlesner M., Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016). 10.1093/bioinformatics/btw313. PubMed DOI

Guindon S., et al. , New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010). PubMed

Metscher B. D., MicroCT for developmental biology: A versatile tool for high-contrast 3D imaging at histological resolutions. Dev. Dyn. 238, 632–640 (2009). PubMed

Connolly M. H., Yelick P. C., High-throughput methods for visualizing the teleost skeleton: Capturing autofluorescence of alizarin red. J. Appl. Ichthyol. 26, 274–277 (2010).

Stundl J., et al. , Ancient vertebrate dermal armor evolved from trunk neural crest. NCBI Gene Expression Omnibus. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE235280. Deposited 24 June 2023. PubMed PMC

Generation of a zebrafish neurofibromatosis model via inducible knockout of nf2a/b

Identification of multiple transcription factor genes potentially involved in the development of electrosensory versus mechanosensory lateral line organs

Ancient vertebrate dermal armor evolved from trunk neural crest