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Potential contribution of intrinsic developmental stability toward body plan conservation
BACKGROUND: Despite the morphological diversity of animals, their basic anatomical patterns—the body plans in each animal phylum—have remained highly conserved over hundreds of millions of evolutionary years. This is attributed to conservation of the body plan-establishing developmental period (the...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2022
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8996622/ https://www.ncbi.nlm.nih.gov/pubmed/35399082 http://dx.doi.org/10.1186/s12915-022-01276-5 |
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author | Uchida, Yui Shigenobu, Shuji Takeda, Hiroyuki Furusawa, Chikara Irie, Naoki |
author_facet | Uchida, Yui Shigenobu, Shuji Takeda, Hiroyuki Furusawa, Chikara Irie, Naoki |
author_sort | Uchida, Yui |
collection | PubMed |
description | BACKGROUND: Despite the morphological diversity of animals, their basic anatomical patterns—the body plans in each animal phylum—have remained highly conserved over hundreds of millions of evolutionary years. This is attributed to conservation of the body plan-establishing developmental period (the phylotypic period) in each lineage. However, the evolutionary mechanism behind this phylotypic period conservation remains under debate. A variety of hypotheses based on the concept of modern synthesis have been proposed, such as negative selection in the phylotypic period through its vulnerability to embryonic lethality. Here we tested a new hypothesis that the phylotypic period is developmentally stable; it has less potential to produce phenotypic variations than the other stages, and this has most likely led to the evolutionary conservation of body plans. RESULTS: By analyzing the embryos of inbred Japanese medaka embryos raised under the same laboratory conditions and measuring the whole embryonic transcriptome as a phenotype, we found that the phylotypic period has greater developmental stability than other stages. Comparison of phenotypic differences between two wild medaka populations indicated that the phylotypic period and its genes in this period remained less variational, even after environmental and mutational modifications accumulated during intraspecies evolution. Genes with stable expression levels were enriched with those involved in cell-cell signalling and morphological specification such as Wnt and Hox, implying possible involvement in body plan development of these genes. CONCLUSIONS: This study demonstrated the correspondence between the developmental stage with low potential to produce phenotypic variations and that with low diversity in micro- and macroevolution, namely the phylotypic period. Whereas modern synthesis explains evolution as a process of shaping of phenotypic variations caused by mutations, our results highlight the possibility that phenotypic variations are readily limited by the intrinsic nature of organisms, namely developmental stability, thus biasing evolutionary outcomes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01276-5. |
format | Online Article Text |
id | pubmed-8996622 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-89966222022-04-12 Potential contribution of intrinsic developmental stability toward body plan conservation Uchida, Yui Shigenobu, Shuji Takeda, Hiroyuki Furusawa, Chikara Irie, Naoki BMC Biol Research Article BACKGROUND: Despite the morphological diversity of animals, their basic anatomical patterns—the body plans in each animal phylum—have remained highly conserved over hundreds of millions of evolutionary years. This is attributed to conservation of the body plan-establishing developmental period (the phylotypic period) in each lineage. However, the evolutionary mechanism behind this phylotypic period conservation remains under debate. A variety of hypotheses based on the concept of modern synthesis have been proposed, such as negative selection in the phylotypic period through its vulnerability to embryonic lethality. Here we tested a new hypothesis that the phylotypic period is developmentally stable; it has less potential to produce phenotypic variations than the other stages, and this has most likely led to the evolutionary conservation of body plans. RESULTS: By analyzing the embryos of inbred Japanese medaka embryos raised under the same laboratory conditions and measuring the whole embryonic transcriptome as a phenotype, we found that the phylotypic period has greater developmental stability than other stages. Comparison of phenotypic differences between two wild medaka populations indicated that the phylotypic period and its genes in this period remained less variational, even after environmental and mutational modifications accumulated during intraspecies evolution. Genes with stable expression levels were enriched with those involved in cell-cell signalling and morphological specification such as Wnt and Hox, implying possible involvement in body plan development of these genes. CONCLUSIONS: This study demonstrated the correspondence between the developmental stage with low potential to produce phenotypic variations and that with low diversity in micro- and macroevolution, namely the phylotypic period. Whereas modern synthesis explains evolution as a process of shaping of phenotypic variations caused by mutations, our results highlight the possibility that phenotypic variations are readily limited by the intrinsic nature of organisms, namely developmental stability, thus biasing evolutionary outcomes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01276-5. BioMed Central 2022-04-11 /pmc/articles/PMC8996622/ /pubmed/35399082 http://dx.doi.org/10.1186/s12915-022-01276-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Uchida, Yui Shigenobu, Shuji Takeda, Hiroyuki Furusawa, Chikara Irie, Naoki Potential contribution of intrinsic developmental stability toward body plan conservation |
title | Potential contribution of intrinsic developmental stability toward body plan conservation |
title_full | Potential contribution of intrinsic developmental stability toward body plan conservation |
title_fullStr | Potential contribution of intrinsic developmental stability toward body plan conservation |
title_full_unstemmed | Potential contribution of intrinsic developmental stability toward body plan conservation |
title_short | Potential contribution of intrinsic developmental stability toward body plan conservation |
title_sort | potential contribution of intrinsic developmental stability toward body plan conservation |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8996622/ https://www.ncbi.nlm.nih.gov/pubmed/35399082 http://dx.doi.org/10.1186/s12915-022-01276-5 |
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