Set‐aside cells in maximal indirect development: Evolutionary and developmental significance
Abstract
In the maximal form of indirect development found in many taxa of marine invertebrates, embryonic cell lineages of fixed fate and limited division capacity give rise to the larval structures. The adult arises from set‐aside cells in the larva that are held out from the early embryonic specification processes, and that retain extensive proliferative capacity. We review the locations and fates of set‐aside cells in two protostomes, a lophophorate and a deuterostome. The distinct adult body plans of many phyla develop from homologous set‐aside cells within homologous larvae. We argue that the stocks from which these phyla arose utilized these respective larvae, and the diversity of their adult body plans reflects diverse pattern formation processes executed in their set‐aside cell populations. Chordates and arthropods develop directly, but share adult characters with indirectly developing phyla. Thus the deuterostome and protostome stocks that were ancestral to chordates and arthropods, respectively, also utilized maximal indirect development.
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For deuterostomes and lophotrochozoans, maximal indirect development is primitive, and direct development is derived.
“Many lines of evidence show that for deuterostomes and lophotrochozoans maximal indirect development is primitive, and direct development is derived (36–38).”
From Precambrian animal diversity: Putative phosphatized embryos from the Doushantuo Formation of China (2000) · cites this paper as [36]
In maximal indirect development, the adult body plan forms within the larva from special patches of cells set aside during embryogenesis.
“In maximal indirect development, the adult body plan instead forms within the larva by a complex secondary process from special patches of cells set aside during embryogenesis (1).”
From Expression of the <i>Hox</i> gene complex in the indirect development of a sea urchin (1998) · cites this paper as [1]
Indirect development is primitive for bilaterians.
“We have discussed elsewhere evidence that has led us and our colleagues to conclude that indirect development is primitive for bilaterians (1, 5).”
From Expression of the <i>Hox</i> gene complex in the indirect development of a sea urchin (1998) · cites this paper as [1]
In maximal indirect development, the embryo produces a larva that bears little relation to the adult body plan, and the adult is formed by a separate postembryonic developmental process.
“In maximal indirect development, as defined earlier (Davidson et al., 1995;Peterson et al., 1997), the embryo gives rise to a larva that bears little relation to the adult body plan, and the latter is formed by a separate postembryonic developmental process.”
From Bilaterian Origins: Significance of New Experimental Observations (2000) · cites this paper as Peterson et al., 1997
The latest common ancestor of hemichordates and echinoderms would also have expressed Brachyury in its mesodermal set-aside cells.
“In addition it would have expressed the Brachyury gene in its mesodermal set-aside cells (Peterson et al., 1999a,b), supporting the obvious morphological homology of these cells and their coelomic derivatives (Peterson et al., 1997).”
From Bilaterian Origins: Significance of New Experimental Observations (2000) · cites this paper as Peterson et al., 1997
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Self-citationIntroduction: Larval Development, Evolution, and Ecology
Hall, B., & Wake, M. (1999) · Elsevier eBooks · doi:10.1016/b978-012730935-4/50002-x · Cited by 22 · see citing works
Chandramouli, K., Mok, F. S., Wang, H., & Qian, P. (2011) · BMC Developmental Biology · doi:10.1186/1471-213x-11-31 · Cited by 31 · see citing works
Cilia propel the embryo in the right direction
Brueckner, M. K. (2001) · American Journal of Medical Genetics · doi:10.1002/1096-8628(20010715)101:4 · Cited by 90 · see citing works
Mok, F. S., Thiyagarajan, V., & Qian, P. (2009) · Proteome Science · doi:10.1186/1477-5956-7-44 · Cited by 30 · see citing works
Neuroectodermal and endodermal expression of the ascidian Cdx gene is separated by metamorphosis
Hinman, V. F., Becker, E., & Degnan, B. M. (2000) · Development Genes and Evolution · doi:10.1007/s004270050306 · Cited by 30 · see citing works
Evolutionary developmental biology (evo-devo) of cestodes
Koziol, U. (2016) · Experimental Parasitology · doi:10.1016/j.exppara.2016.12.004 · Cited by 29 · see citing works
Temereva, E. N., & Malakhov, V. V. (2015) · BMC Evolutionary Biology · doi:10.1186/s12862-015-0504-0 · Cited by 29 · see citing works
An evolutionary transition of vasa regulation in echinoderms
Juliano, C. E., & Wessel, G. M. (2009) · Evolution & Development · doi:10.1111/j.1525-142x.2009.00362.x · Cited by 29 · see citing works
The evolution of embryonic patterning mechanisms in animals
Wray, G. A. (2000) · Seminars in Cell and Developmental Biology · doi:10.1006/scdb.2000.0191 · Cited by 29 · see citing works
Gilbert, E., Teeling, C., Lebedeva, T. S., Pedersen, S., Chrismas, N. A. M., Genikhovich, G., & Modepalli, V. (2022) · Development · doi:10.1242/dev.200833 · Cited by 26 · see citing works
MicroRNAs support the monophyly of enteropneust hemichordates
Peterson, K. J., Su, Y., Arnone, M. I., Swalla, B. J., & King, B. L. (2013) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22510 · Cited by 27 · see citing works
Self-citationA new computational growth model for sea urchin skeletons
Zachos, L. G. (2009) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2009.04.007 · Cited by 27 · see citing works
Genetic aspects of atrioventricular septal defects
Pierpont, M. E., Markwald, R. R., & Lin, A. E. (2000) · American Journal of Medical Genetics · doi:10.1002/1096-8628(200024)97:4 · Cited by 75 · see citing works
Morphological and ultrastructural analysis of Turritopsis nutricula during life cycle reversal
Carlà, E. C., Pagliara, P., Piraino, S., Boero, F., & Dini, L. (2003) · Tissue and Cell · doi:10.1016/s0040-8166(03)00028-4 · Cited by 26 · see citing works
Stem Cells in Aquatic Invertebrates: Common Premises and Emerging Unique Themes
Rinkevich, Y., Matranga, V., & Rinkevich, B. (2009) · Springer eBooks · doi:10.1007/978-90-481-2767-2_4 · Cited by 26 · see citing works
Yamaguchi, E., & Seaver, E. C. (2013) · Invertebrate Biology · doi:10.1111/ivb.12034 · Cited by 24 · see citing works
Page, L. R. (2000) · Evolution & Development · doi:10.1046/j.1525-142x.2000.00017.x · Cited by 23 · see citing works
Not all written in stone: interdisciplinary syntheses in echinoderm paleontology
Mooi, R. (2001) · Canadian Journal of Zoology · doi:10.1139/z00-217 · Cited by 23 · see citing works
- Authors
- Peterson, K. J., Cameron, R. A., & Davidson, E. H.
- Affiliations
- California Institute of Technology (US)
- Venue
- BioEssays
- Publisher
- Wiley
- Published
- 1997-07
- Volume
- 19
- Issue
- 7
- Pages
- 623-631
- ISSN
- 0265-9247 (ISSN-L)
- 1521-1878
- OpenAlex
- W2091430768
- Semantic Scholar
- 1f5d5b8085a17fa2183504b7ec2e7338f404df75
- Cited by
- 164
- References
- 25
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 1 · 2023: 6 · 2022: 8 · 2020: 2 · 2019: 3 · 2018: 3 · 2017: 1 · 2016: 7 · 2015: 7 · 2014: 5 · 2013: 4
- FWCI
- 1.07
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- BioEssays (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- National Institutes of Health
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD05753)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Planarian Biology and Electrostimulation
- Keywords
- larval development, embryonic cell lineage, pattern formation, protostomes, deuterostomes, lophophorates, chordate evolution, arthropod evolution, body plan evolution
- MeSH terms
- Animals, Arthropods, Chordata, Nonvertebrate, Biological Evolution, Invertebrates, Larva, Morphogenesis, Phylogeny, Species Specificity, Stem Cells, Cell Lineage
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