Inherency of Form and Function in Animal Development and Evolution
I discuss recent work on the origins of morphology and cell-type diversification in Metazoa – collectively the animals – and propose a scenario for how these two properties became integrated, with the help of a third set of processes, cellular pattern formation, into the developmental programs seen...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-06-01
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| Series: | Frontiers in Physiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fphys.2019.00702/full |
| _version_ | 1818359379896827904 |
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| author | Stuart A. Newman |
| author_facet | Stuart A. Newman |
| author_sort | Stuart A. Newman |
| collection | DOAJ |
| description | I discuss recent work on the origins of morphology and cell-type diversification in Metazoa – collectively the animals – and propose a scenario for how these two properties became integrated, with the help of a third set of processes, cellular pattern formation, into the developmental programs seen in present-day metazoans. Inherent propensities to generate familiar forms and cell types, in essence a parts kit for the animals, are exhibited by present-day organisms and were likely more prominent in primitive ones. The structural motifs of animal bodies and organs, e.g., multilayered, hollow, elongated and segmented tissues, internal and external appendages, branched tubes, and modular endoskeletons, can be accounted for by the properties of mesoscale masses of metazoan cells. These material properties, in turn, resulted from the recruitment of “generic” physical forces and mechanisms – adhesion, contraction, polarity, chemical oscillation, diffusion – by toolkit molecules that were partly conserved from unicellular holozoan antecedents and partly novel, distributed in the different metazoan phyla in a fashion correlated with morphological complexity. The specialized functions of the terminally differentiated cell types in animals, e.g., contraction, excitability, barrier function, detoxification, excretion, were already present in ancestral unicellular organisms. These functions were implemented in metazoan differentiation in some cases using the same transcription factors as in single-celled ancestors, although controlled by regulatory mechanisms that were hybrids between earlier-evolved processes and regulatory innovations, such as enhancers. Cellular pattern formation, mediated by released morphogens interacting with biochemically responsive and excitable tissues, drew on inherent self-organizing processes in proto-metazoans to transform clusters of holozoan cells into animal embryos and organs. |
| first_indexed | 2024-12-13T20:43:58Z |
| format | Article |
| id | doaj.art-b4b2a2e3d8d747baa9ae938880e33715 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-13T20:43:58Z |
| publishDate | 2019-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-b4b2a2e3d8d747baa9ae938880e337152022-12-21T23:32:05ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2019-06-011010.3389/fphys.2019.00702443732Inherency of Form and Function in Animal Development and EvolutionStuart A. NewmanI discuss recent work on the origins of morphology and cell-type diversification in Metazoa – collectively the animals – and propose a scenario for how these two properties became integrated, with the help of a third set of processes, cellular pattern formation, into the developmental programs seen in present-day metazoans. Inherent propensities to generate familiar forms and cell types, in essence a parts kit for the animals, are exhibited by present-day organisms and were likely more prominent in primitive ones. The structural motifs of animal bodies and organs, e.g., multilayered, hollow, elongated and segmented tissues, internal and external appendages, branched tubes, and modular endoskeletons, can be accounted for by the properties of mesoscale masses of metazoan cells. These material properties, in turn, resulted from the recruitment of “generic” physical forces and mechanisms – adhesion, contraction, polarity, chemical oscillation, diffusion – by toolkit molecules that were partly conserved from unicellular holozoan antecedents and partly novel, distributed in the different metazoan phyla in a fashion correlated with morphological complexity. The specialized functions of the terminally differentiated cell types in animals, e.g., contraction, excitability, barrier function, detoxification, excretion, were already present in ancestral unicellular organisms. These functions were implemented in metazoan differentiation in some cases using the same transcription factors as in single-celled ancestors, although controlled by regulatory mechanisms that were hybrids between earlier-evolved processes and regulatory innovations, such as enhancers. Cellular pattern formation, mediated by released morphogens interacting with biochemically responsive and excitable tissues, drew on inherent self-organizing processes in proto-metazoans to transform clusters of holozoan cells into animal embryos and organs.https://www.frontiersin.org/article/10.3389/fphys.2019.00702/fullbiogenericmorphogenesispattern formationcell differentiationself-organizationphase transition |
| spellingShingle | Stuart A. Newman Inherency of Form and Function in Animal Development and Evolution Frontiers in Physiology biogeneric morphogenesis pattern formation cell differentiation self-organization phase transition |
| title | Inherency of Form and Function in Animal Development and Evolution |
| title_full | Inherency of Form and Function in Animal Development and Evolution |
| title_fullStr | Inherency of Form and Function in Animal Development and Evolution |
| title_full_unstemmed | Inherency of Form and Function in Animal Development and Evolution |
| title_short | Inherency of Form and Function in Animal Development and Evolution |
| title_sort | inherency of form and function in animal development and evolution |
| topic | biogeneric morphogenesis pattern formation cell differentiation self-organization phase transition |
| url | https://www.frontiersin.org/article/10.3389/fphys.2019.00702/full |
| work_keys_str_mv | AT stuartanewman inherencyofformandfunctioninanimaldevelopmentandevolution |