Abstract
As proposed by Wilhelm Roux in 1885, the key goal of experimental embryology (“Entwicklungsmechanik”) was to elucidate whether organisms or their parts develop autonomously (“self-differentiation”) or require interactions with other parts or the environment. However, experimental embryologists soon realized that concepts like “self-differentiation” only make sense when applied to particular parts or units of the developing embryo as defined both in time and space. Whereas the formation of tissues or organs may initially depend on interactions with surrounding tissues, they later become independent of such interactions or “determined.” Moreover, the determination of a particular tissue or organ primordium has to be distinguished from the spatially coordinated determination of its parts—what we now refer to as “patterning.” While some primordia depend on extrinsic influences (e.g., signals from adjacent tissues) for proper patterning, others rely on intrinsic mechanisms. Such intrinsically patterned units may behave as “morphogenetic fields” that can compensate for lost parts and regulate their size and proper patterning. While these insights were won by experimental embryologists more than 100 years ago, they retain their relevance today. To enable the generation of more life-like organoids in vitro for studying developmental processes and diseases in a dish, questions about the spatiotemporal units of development (when and how tissues and organs are determined and patterned) need to be increasingly considered. This review briefly sketches this conceptual history and its continued relevance by focusing on the determination and patterning of the inner ear with a specific emphasis on some studies published in this journal.
Similar content being viewed by others
Data availability
Not applicable
References
Abello G, Alsina B (2007) Establishment of a proneural field in the inner ear. Int J Dev Biol 51:483–493
Ben-Zvi D, Shilo BZ, Barkai N (2011) Scaling of morphogen gradients. Curr Opin Genet Dev 21:704–710
Braus H (1904) Einige Ergebnisse der Transplantation von Organanlagen bei Bombinatorlarven. Verh d Anatom Ges 18:53–66
Clevers H (2016) Modeling development and disease with organoids. Cell 165:1586–1597
De Robertis EM, Morita EA, Cho KWY (1991) Gradient fields and homeobox genes. Development 112:669–678
Delgado I, Torres M (2017) Coordination of limb development by crosstalk among axial patterning pathways. Dev Biol 429:382–386
Driesch H (1891) Entwicklungsmechanische Studien. I. Der Werth der beiden ersten Furchungszellen in der Echinodermenentwicklung. Experimentelle Erzeugen von Theil-und Doppelbildungen. Z Zool 53:160–178
Driesch H (1899) Die lokalisation morphogenetischer vorgänge. Ein beweis vitalistischen geschehens. Archiv für Entwicklungsmechanik 8:35–111
Eiraku M, Takata N, Ishibashi H, Kawada M, Sakakura E, Okuda S, Sekiguchi K, Adachi T et al (2011) Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472:51–56
Eisinger K, Sternberg H (1923) Beiträge zur Entwicklungsmechanik des inneren Ohres. Archiv f mikrosk Anat u Entwcklungsmechanik 100:542–559
Fritzsch B, Barald KF, Lomax MI (1998) Early embryology of the vertebrate ear. In: Rubel EW, Popper AN, Fay RR (eds) Development of the auditory system. Springer, New York, pp 80–145
Ginsburg AS (1995) Determination of the labyrinth in different amphibina species and its correlation with determination of the other ectoderm derivatives. Roux’s Arch Dev Biol 204:351–358
Groves AK, Fekete DM (2012) Shaping sound in space: the regulation of inner ear patterning. Development 139:245–257
Harrison RG (1907) Experiments in transplanting limbs and their bearing upon the problems of the development of nerves. J Exp Zool 4:239–281
Harrison RG (1918) Experiments on the development of the fore limb of Amblystoma, a self-differentiating, equipotential system. J Exp Zool 25:413–461
Harrison RG (1924) Experiments on the development of the internal ear. Science 59:448
Harrison RG (1936) Relations of symmetry in the developing ear of Amblystoma punctatum. Proc Natl Acad Sci USA 22:238–247
Harrison RG (1969) Harrison stages and description of the normal development of the spotted salamander, Amblystoma punctatum (Linn.). In: Harrison RG (ed) Organization and development of the embryo. New Haven, Yale University Press
Hollinshead WH (1932) Determination of potencies in the forelimb of Amblystoma punctatum. J Exp Zool 73:183–194
Huxley JS, de Beer GR (1934) The elements of experimental embryology. Cambridge University Press, Cambridge
Kaan HW (1927) Experiments on the development of the ear of Amblystoma punctatum. J ExpZool 46:13–61
Kicheva A, Briscoe J (2015) Developmental pattern formation in phases. Trends Cell Biol 25:579–591
Maienschein J (2014) Embryos under the microscope. MA, Harvard University Press, Cambridge
Plouhinec JL, De Robertis EM (2009) Systems biology of the self-regulating morphogenetic gradient of the Xenopus gastrula. Cold Spring Harb Perspect Biol 1:a001701
Raft S, Groves AK (2015) Segregating neural and mechanosensory fates in the developing ear: patterning, signaling, and transcriptional control. Cell Tissue Res 359:315–332
Roccio M, Edge ASB (2019) Inner ear organoids: new tools to understand neurosensory cell development, degeneration and regeneration. Development 146:dev177188
Röhlich K (1929) Experimentelle untersuchungen über den zeitpunkt der determination der gehörblase bei Amblystoma-Embryonen. Wilhelm Roux’ Archiv für Entwicklungsmechanik der Organismen 118:164–199
Roux W (1885) Beiträge zur Entwickelungsmechanik des Embryos. I. Zur Orientirung über einige Probleme der organischen Entwickelung. Z Biol 21:411–524
Roux W (1888) Beiträge zur Entwickelungsmechanik des Embryo. V. Ueber die künstliche Hervorbringung “halber” Embryonen durch Zerstörung einer der beiden ersten Furchungszellen, sowie über die Nachentwickelung (Post generation) der fehlenden Körperhälfte. Virchow’s Archiv 114:419–521
Saha M (1991) Spemann seen through a lens. In: Gilbert SF (ed) A conceptual history of modern embryology. Plenum Press, New York, pp 91–108
Sasai Y (2013) Cytosystems dynamics in self-organization of tissue architecture. Nature 493:318–326
Schaper A (1904) Über einige fälle atypischer linsenentwicklung unter abnormen bedingungen. Anat Anz 24:305–326
Schlosser G (2021) Development of sensory and neurosecretory cell types. Vertebrate cranial placodes, Vol.1. Boca Raton. CRC Press
Simunovic M, Brivanlou AH (2017) Embryoids, organoids and gastruloids: new approaches to understanding embryogenesis. Development 144:976–985
Slack JMW (1991) From egg to embryo. Cambridge Univ, Press, Cambridge
Spemann H (1901) Ueber Correlationen in der Entwicklung des Auges. Verh Anat Ges 15:61–79
Spemann H (1905) Über Linsenbildung nach experimenteller Entfernung der primären Linsenbildungszellen. Zool Anzeiger 28:419–432
Spemann H (1906) Über eine neue Methode der embryonalen Transplantation. Verhand Deutsch Zool Gesellsch 16:195–202
Spemann H (1910) Die Entwicklung des invertierten Hörgrübchens zum Labyrinth. Archiv für Entwicklungsmechanik 30:437–458
Spemann H (1918) Über die Determination der ersten Organanlagen des Amphibienembryo. Archiv für Entwicklungsmechanik 43:448–555
Spemann H (1921) Die Erzeugung tierischer Chimären durch heteroplastische embryonale Transplantationen zwischen Triton cristatus und taeniatus. Roux Arch Entwickl mech 48:533–570
Spemann H (1936) Experimentelle Beiträge zu einer Theorie der Entwicklung. Springer, Berlin
Spemann H, Geinitz B (1927) Über Weckung organisatorischer Fähigkeiten durch Verpflanzung in organisatorische Umgebung. Archiv für Entwicklungsmechanik 109:129–175
Stocum DL, Fallon JF (1982) Control of pattern formation in urodele limb ontogeny: a review and a hypothesis. J Embryol Exp Morphol 69:7–36
Streeter GL (1907) Some factors in the development of the amphibian ear vesicle and further experiments on equilibration. J Exp Zool 4:431–445
van der Valk WH, Steinhart MR, Zhang J, Koehler KR (2021) Building inner ears: recent advances and future challenges for in vitro organoid systems. Cell Death Differ 28:24–34
Weismann A (1885) Die Continuität des Keimplasma’s als Grundlage einer Theorie der Vererbung. Jena, Gustav Fischer
Weiss P (1939) Principles of development. Henry Holt and Co, New York
Wolpert L (1969) Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25:1–47
Wu DK, Kelley MW (2012) Molecular mechanisms of inner ear development. Cold Spring Harb Perspect Biol 4:a008409
Yntema CL (1933) Experiments on the determination of the ear ectoderm in the embryo of Amblystoma punctatum. J Exp Zool 65:317–357
Yntema CL (1939) Self-differentiation of heterotopic ear ectoderm in the embryo of Amblystoma punctatum. J Exp Zool 80:1–17
Zuniga A (2015) Next generation limb development and evolution: old questions, new perspectives. Development 142:3810–3820
Funding
None.
Author information
Authors and Affiliations
Contributions
G.S wrote the manuscript and prepared the figures.
Corresponding author
Ethics declarations
Competing interests
The author declares no competing interests.
Additional information
Responsible Editor: V. Hartenstein
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Schlosser, G. From “self-differentiation” to organoids—the quest for the units of development. Dev Genes Evol (2023). https://doi.org/10.1007/s00427-023-00711-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00427-023-00711-z