The DOI matches its Crossref record; 88 of the 88 references it cites were found in a registry or an index.
Mechanisms of pattern formation in development and evolution
Abstract
We present a classification of developmental mechanisms that have been shown experimentally to generate pattern and form in metazoan organisms. We propose that all such mechanisms can be organized into three basic categories and that two of these may act as composite mechanisms in two different ways. The simple categories are cell autonomous mechanisms in which cells enter into specific arrangements (`patterns') without interacting, inductive mechanisms in which cell communication leads to changes in pattern by reciprocal or hierarchical alteration of cell phenotypes (`states')and morphogenetic mechanisms in which pattern changes by means of cell interactions that do not change cell states. The latter two types of mechanism can be combined either morphostatically, in which case inductive mechanisms act first, followed by the morphogenetic mechanism, or morphodynamically, in which case both types of mechanisms interact continuously to modify each other's dynamics. We propose that this previously unexplored distinction in the operation of composite developmental mechanisms provides insight into the dynamics of many developmental processes. In particular, morphostatic and morphodynamic mechanisms respond to small changes in their genetic and microenvironmental components in dramatically different ways. We suggest that these differences in `variational properties' lead to morphostatic and morphodynamic mechanisms being represented to different extents in early and late stages of development and to their contributing in distinct ways to morphological transitions in evolution.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The chemical basis of morphogenesis
Turing, A. M. (1952) · Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences · doi:10.1098/rstb.1952.0012 · Cited by 11,733
Positional information and the spatial pattern of cellular differentiation
Wolpert, L. (1969) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(69)80016-0 · Cited by 3,050
Le Douarin, N., & Kalcheim, C. (1999) · Cambridge University Press eBooks · doi:10.1017/cbo9780511897948 · Cited by 3,014
A genomic regulatory network for development
Davidson, E. H., Rast, J. P., Oliveri, P., Ransick, A., Calestani, C., Yuh, C.-H., Minokawa, T., Amore, G., Hinman, V., Arenas-Mena, C., et al. (2002) · Science · doi:10.1126/science.1069883 · Cited by 1,567
The segment polarity network is a robust developmental module
von Dassow, G., Meir, E., Munro, E. M., & Odell, G. M. (2000) · Nature · doi:10.1038/35018085 · Cited by 1,144
Reiterative signaling and patterning during mammalian tooth morphogenesis
Jernvall, J., & Thesleff, I. (2000) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00322-6 · Cited by 1,103
Self-citationBrault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D. H., McMahon, A. P., Sommer, L., Boussadia, O., & Kemler, R. (2001) · Development · doi:10.1242/dev.128.8.1253 · Cited by 1,088
Meier, P., Finch, A., & Evan, G. (2000) · Nature · doi:10.1038/35037734 · Cited by 1,039
FORMATION AND FUNCTION OF SPEMANN'S ORGANIZER
Harland, R., & Gerhart, J. (1997) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.13.1.611 · Cited by 839
A reaction–diffusion wave on the skin of the marine angelfish Pomacanthus
Kondo, S., & Asai, R. (1995) · Nature · doi:10.1038/376765a0 · Cited by 806
Evolution of genetic redundancy
Nowak, M. A., Boerlijst, M. C., Cooke, J., & Smith, J. M. (1997) · Nature · doi:10.1038/40618 · Cited by 764
Dominoes and Clocks: the Union of Two Views of the Cell Cycle
Murray, A. W., & Kirschner, M. W. (1989) · Science · doi:10.1126/science.2683077 · Cited by 729
Structural Stability And Morphogenesis
(2018) · CRC Press eBooks · doi:10.1201/9780429493027 · Cited by 622
Pattern formation by local self-activation and lateral inhibition
Meinhardt, H., & Gierer, A. (2000) · BioEssays · doi:10.1002/1521-1878(200008)22:8<753::aid-bies9>3.0.co;2-z · Cited by 615
Maturational disturbance of chondrocytes inCbfa1-deficient mice
Inada, M., Yasui, T., Nomura, S., Miyake, S., Deguchi, K., Himeno, M., Sato, M., Yamagiwa, H., Kimura, T., Yasui, N., et al. (1999) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199904)214:4<291::aid-aja2>3.0.co;2-e · Cited by 572
REGIONALIZATION OF THE PROSENCEPHALIC NEURAL PLATE
Rubenstein, J. L. R., Shimamura, K., Martinez, S., & Puelles, L. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.445 · Cited by 550
Mechanisms of convergence and extension by cell intercalation
Keller, R., Davidson, L., Edlund, A., Elul, T., Ezin, M., Shook, D., & Skoglund, P. (2000) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2000.0626 · Cited by 519
Jernvall, J., Åberg, T., Kettunen, P., Keränen, S., & Thesleff, I. (1998) · Development · doi:10.1242/dev.125.2.161 · Cited by 445
Self-citationMechanisms of programmed cell death in the developing brain
Kuan, C.-Y., Roth, K. A., Flavell, R. A., & Rakic, P. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01581-2 · Cited by 443
Jernvall, J., Kettunen, P., Karavanova, I., Martin, L. B., & Thesleff, I. (1994) · The International Journal of Developmental Biology · doi:10.1387/ijdb.7848830 · Cited by 435
Self-citationA connectionist model of development
Mjolsness, E., Sharp, D. H., & Reinitz, J. (1991) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80391-1 · Cited by 434
A gene network model accounting for development and evolution of mammalian teeth
Salazar-Ciudad, I., & Jernvall, J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.132069499 · Cited by 393
Self-citationDevelopment of the Vertebrate Cornea
Hay, E. D. (1980) · International Review of Cytology · doi:10.1016/s0074-7696(08)61760-x · Cited by 388
EVOLUTION AND BIFURCATION OF DEVELOPMENTAL PROGRAMS
Oster, G., & Alberch, P. (1982) · Evolution · doi:10.1111/j.1558-5646.1982.tb05066.x · Cited by 379
Developmental Constraints in Evolutionary Processes
Alberch, P. (1982) · Evolution and Development · doi:10.1007/978-3-642-45532-2_15 · Cited by 376
Order in Living Organisms: A Systems Analysis of Evolution.
Harper, C. W., & Riedl, R. (1980) · Systematic Zoology · doi:10.2307/2412636 · Cited by 354
Mlodzik, M. (2002) · Trends in Genetics · doi:10.1016/s0168-9525(02)02770-1 · Cited by 341
Sequential actions of BMP receptors control neural precursor cell production and fate
Panchision, D. M., Pickel, J. M., Studer, L., Lee, S.-H., Turner, P. A., Hazel, T. G., & McKay, R. D. G. (2001) · Genes & Development · doi:10.1101/gad.894701 · Cited by 327
Positional information revisited
Wolpert, L. (1989) · Development · doi:10.1242/dev.107.supplement.3 · Cited by 325
Pax6 Modulates the Dorsoventral Patterning of the Mammalian Telencephalon
Stoykova, A., Treichel, D., Hallonet, M., & Gruss, P. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08042.2000 · Cited by 316
Epigenetic mechanisms of character origination
Newman, S. A., & M�ller, G. B. (2000) · Journal of Experimental Zoology · doi:10.1002/1097-010x(20001215)288:4<304::aid-jez3>3.0.co;2-g · Cited by 304
Self-citationA re-examination of proximodistal patterning during vertebrate limb development
Dudley, A. T., Ros, M. A., & Tabin, C. J. (2002) · Nature · doi:10.1038/nature00945 · Cited by 294
Linking development with generation of novelty in mammalian teeth
Jernvall, J. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.050586297 · Cited by 293
Self-citationBUTLER, P. M. (1956) · Biological Reviews · doi:10.1111/j.1469-185x.1956.tb01551.x · Cited by 292
Associations of FGF-3 and FGF-10 with signaling networks regulating tooth morphogenesis
Kettunen, P. J., Laurikkala, J., Itäranta, P., Vainio, S. J., Itoh, N., & Thesleff, I. (2000) · Developmental Dynamics · doi:10.1002/1097-0177(2000)9999:9999<::aid-dvdy1062>3.0.co;2-j · Cited by 280
Axis formation during Drosophila oogenesis
Riechmann, V., & Ephrussi, A. (2001) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00207-0 · Cited by 274
Dynamics of Skeletal Pattern Formation in Developing Chick Limb
Newman, S. A., & Frisch, H. L. (1979) · Science · doi:10.1126/science.462174 · Cited by 274
Self-citationFrom gradients to stripes in Drosophila embryogenesis: filling in the gaps
Rivera-Pomar, R., & Jãckle, H. (1996) · Trends in Genetics · doi:10.1016/0168-9525(96)10044-5 · Cited by 261
Jiang, T.-X., Jung, H.-S., Widelitz, R. B., & Chuong, C.-M. (1999) · Development · doi:10.1242/dev.126.22.4997 · Cited by 237
Msx homeobox genes inhibit differentiation through upregulation of cyclin D1
Hu, G., Lee, H., Price, S. M., Shen, M. M., & Abate-Shen, C. (2001) · Development · doi:10.1242/dev.128.12.2373 · Cited by 209
Carnac, G., Kodjabachian, L., Gurdon, J. B., & Lemaire, P. (1996) · Development · doi:10.1242/dev.122.10.3055 · Cited by 208
Cusp Patterning Defect in Tabby Mouse Teeth and Its Partial Rescue by FGF
Pispa, J., Jung, H.-S., Jernvall, J., Kettunen, P., Mustonen, T., Tabata, M. J., Kere, J., & Thesleff, I. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9514 · Cited by 197
Self-citationEpstein, D. J., McMahon, A. P., & Joyner, A. L. (1999) · Development · doi:10.1242/dev.126.2.281 · Cited by 169
Su, D.-M., Ellis, S., Napier, A., Lee, K., & Manley, N. R. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0342 · Cited by 162
Adhesion in Development: An Historical Overview
Steinberg, M. S. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0312 · Cited by 161
Asymmetric cell division: fly neuroblast meets worm zygote
Doe, C. Q., & Bowerman, B. (2001) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00176-9 · Cited by 159
Salazar‐Ciudad, I., Newman, S. A., & Solé, R. V. (2001) · Evolution & Development · doi:10.1046/j.1525-142x.2001.003002084.x · Cited by 158
Self-citationGene Networks Capable of Pattern Formation: From Induction to Reaction–Diffusion
Salazar‐Ciudad, I., García‐Fernàndez, J., & Solé, R. V. (2000) · Journal of Theoretical Biology · doi:10.1006/jtbi.2000.2092 · Cited by 150
Self-citationGrindley, J. C., Hargett, L. K., Hill, R. E., Ross, A., & Hogan, B. L. M. (1997) · Mechanisms of Development · doi:10.1016/s0925-4773(97)00055-5 · Cited by 150
Roles of Pax-6 in murine diencephalic development
Warren, N., & Price, D. J. (1997) · Development · doi:10.1242/dev.124.8.1573 · Cited by 141
The Dynamic Architecture of a Developing Organism
Beloussov, L. V. (1998) · Springer eBooks · doi:10.1007/978-94-015-8998-7 · Cited by 141
Vertebrate Hox genes and proliferation: an alternative pathway to homeosis?
Duboule, D. (1995) · Current Opinion in Genetics & Development · doi:10.1016/0959-437x(95)90058-o · Cited by 139
Chemotactic migration of mesencephalic neural crest cells in the mouse
Kubota, Y., & Itô, K. (2000) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(200002)217:2<170::aid-dvdy4>3.0.co;2-9 · Cited by 128
Activation of the cytotactin promoter by the homeobox-containing gene Evx-1.
Jones, F. S., Chalepakis, G., Gruss, P., & Edelman, G. M. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.6.2091 · Cited by 119
Miura, T., & Shiota, K. (2000) · Developmental Dynamics · Cited by 118
Salser, S. J., & Kenyon, C. J. (1996) · Development · doi:10.1242/dev.122.5.1651 · Cited by 118
Salazar‐Ciudad, I., Solé, R. V., & Newman, S. A. (2001) · Evolution & Development · doi:10.1046/j.1525-142x.2001.003002095.x · Cited by 107
Self-citationDevelopmental patterns of cartilage
Linda, J. S. (1999) · Frontiers in bioscience · doi:10.2741/sandell · Cited by 103
Ferrari, D., Lichtler, A. C., Pan, Z., Dealy, C. N., Upholt, W. B., & Kosher, R. A. (1998) · Developmental Biology · doi:10.1006/dbio.1998.8880 · Cited by 102
Gañán, Y., Macias, D., Basco, R. D., Merino, R., & Hurlé, J. M. (1998) · Developmental Biology · doi:10.1006/dbio.1997.8843 · Cited by 102
Werb, Z., Sympson, C. J., Alexander, C. M., et al. (1996) · PubMed · Cited by 99
Development and Control of Tissue Separation at Gastrulation in Xenopus
Wacker, S., Grimm, K., Joos, T. O., & Winklbauer, R. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9794 · Cited by 98
Modeling the interplay of generic and genetic mechanisms in cleavage, blastulation, and gastrulation
Drasdo, D., & Forgács, G. (2000) · Developmental Dynamics · doi:10.1002/1097-0177(200010)219:2<182::aid-dvdy1040>3.3.co;2-1 · Cited by 96
Chen, Y., & Zhao, X. (1998) · Journal of Experimental Zoology · doi:10.1002/(sici)1097-010x(19981215)282:6<691::aid-jez5>3.0.co;2-s · Cited by 95
Reaction–diffusion models of within-feather pigmentation patterning
Prum, R. O., & Williamson, S. (2002) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2001.1896 · Cited by 94
The role of cell lineage in development
Stent, G. S. (1985) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1985.0174 · Cited by 90
Chen, Y., & Zhao, X. (1998) · PubMed · Cited by 84
Apoptosis in cardiac development
Poelmann, R. E., Molin, D. G. M., Wisse, L. J., & Groot, A. C. G. (2000) · Cell and Tissue Research · doi:10.1007/s004410000227 · Cited by 78
Intimal thickening involves transdifferentiation of embryonic endothelial cells
Arciniegas, E., Ponce, L., Hartt, Y., Graterol, A., & Carlini, R. G. (2000) · The Anatomical Record · doi:10.1002/(sici)1097-0185(20000101)258:1<100::aid-ar11>3.0.co;2-3 · Cited by 76
Model of Convergent Extension in Animal Morphogenesis
Zajac, M., Jones, G. L., & Glazier, J. A. (2000) · Physical Review Letters · doi:10.1103/physrevlett.85.2022 · Cited by 73
A molecular clock involved in Somite segmentation
Maroto, M., & Pourquié, O. (2001) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(01)51007-8 · Cited by 72
Problems and paradigms: Is segmentation generic?
Newman, S. A. (1993) · BioEssays · doi:10.1002/bies.950150409 · Cited by 68
Self-citationA β-catenin/engrailed chimera selectively suppresses Wnt signaling
Montross, W. T., Ji, H. L., & McCrea, P. D. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.10.1759 · Cited by 67
Lallier, T. E., Deutzmann, R., Perris, R., & Bronner-Fraser, M. E. (1994) · Developmental Biology · doi:10.1006/dbio.1994.1101 · Cited by 57
Cell polarity in the early Caenorhabditis elegans embryo
Bowerman, B. A., & Shelton, C. A. (1999) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(99)80059-8 · Cited by 56
Control of pathfinding by the avian trunk neural crest
Erickson, C. A. (1988) · Development · doi:10.1242/dev.103.supplement.63 · Cited by 56
Drosophila segmentation: Supercomputer simulation of prepattern hierarchy
Hunding, A., Kauffman, S. A., & GOODWIN, B. C. (1990) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80116-x · Cited by 55
Principles of Development, a Text in Experimental Embryology
(1939) · Annals of the Entomological Society of America · doi:10.1093/aesa/32.2.475 · Cited by 52
Epigenetic Mechanisms of Character Origination
Newman, S. A., & Müller, G. B. (2001) · Elsevier eBooks · doi:10.1016/b978-012730055-9/50037-9 · Cited by 45
Self-citationOf mice, frogs and flies: Generation of membrane asymmetries in early development
Müller, H. ‐. J. (2001) · Development Growth & Differentiation · doi:10.1046/j.1440-169x.2001.00587.x · Cited by 37
Collagen type IX and developmentally regulated swelling of the avian primary corneal stroma
Fitch, J. M., Fini, M. E., Beebe, D. C., & Linsenmayer, T. F. (1998) · Developmental Dynamics · Cited by 33
Otx and Emx homeobox genes in brain development
Cecchi, C., Mallamaci, A., & Boncinelli, E. (2000) · The International Journal of Developmental Biology · doi:10.1387/ijdb.11061430 · Cited by 29
Freeman, G. (1976) · Developmental Biology · doi:10.1016/0012-1606(76)90148-2 · Cited by 23
Gene network dynamics and the evolution of development
Solé, R. V., Salazar‐Ciudad, I., & Newman, S. A. (2000) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(00)02000-0 · Cited by 21
Self-citationCloning and characterization of aDictyostelium gene encoding a small GTPase of the Rab11 family
Dragoi, I. A., & O’Halloran, T. J. (1998) · Journal of Cellular Biochemistry · doi:10.1002/(sici)1097-4644(19980701)70:1<22::aid-jcb3>3.0.co;2-5 · Cited by 4
Asymmetric Cell Division and Fate Specification in the Drosophila Central Nervous System
Broadus, J., & Spana, E. P. (1999) · Elsevier eBooks · doi:10.1016/b978-012505255-9/50019-5 · Cited by 2
(2001)
Biologists abandon Popper at their peril
(2000) · doi:10.1002/(sici)1521-1878(200002)22:2
Cited by
Emergent patterns of growth controlled by multicellular form and mechanics
Nelson, C. M., Jean, R. P., Tan, J. L., Liu, W. F., Sniadecki, N. J., Spector, A. A., & Chen, C. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502575102 · Cited by 853
Biological Physics of the Developing Embryo
Forgacs, G., & Newman, S. A. (2005) · doi:10.1017/cbo9780511755576 · Cited by 339
Self-citationNewman, S. A., & Bhat, R. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.072481sn · Cited by 208
Self-citationHierarchical patterning modes orchestrate hair follicle morphogenesis
Glover, J. D., Wells, K. L., Matthäus, F., Painter, K. J., Ho, W., Riddell, J., Johansson, J. A., Ford, M. J., Jahoda, C. A. B., Klika, V., et al. (2017) · PLOS Biology · doi:10.1371/journal.pbio.2002117 · Cited by 155
Metadata
- Authors
- Salazar-Ciudad, I., Jernvall, J., & Newman, S. A.
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2003-05-15
- Volume
- 130
- Issue
- 10
- Pages
- 2027-2037
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- OpenAlex
- W2112966482
- Cited by
- 334
- References
- 88
- FWCI
- 5.36
- Type
- journal article
- Language
- en
- Open access
- closed
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.