The DOI matches its Crossref record; 24 of the 24 references it cites were found in a registry or an index.
The Origins of Multicellularity and the Early History of the Genetic Toolkit For Animal Development
Abstract
Multicellularity appeared early and repeatedly in life's history; its instantiations presumably required the confluence of environmental, ecological, and genetic factors. Comparisons of several independently evolved pairs of multicellular and unicellular relatives indicate that transitions to multicellularity are typically associated with increases in the numbers of genes involved in cell differentiation, cell-cell communication, and adhesion. Further examination of the DNA record suggests that these increases in gene complexity are the product of evolutionary innovation, tinkering, and expansion of genetic material. Arguably, the most decisive multicellular transition was the emergence of animals. Decades of developmental work have demarcated the genetic toolkit for animal multicellularity, a select set of a few hundred genes from a few dozen gene families involved in adhesion, communication, and differentiation. Examination of the DNA records of the earliest-branching animal phyla and their closest protist relatives has begun to shed light on the origins and assembly of this toolkit. Emerging data favor a model of gradual assembly, with components originating and diversifying at different time points prior to or shortly after the origin of animals.
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
Evolution of genes and genomes on the Drosophila phylogeny
Drosophila 12 Genomes Consortium (2007) · Nature · doi:10.1038/nature06341 · Cited by 2,010
Broad phylogenomic sampling improves resolution of the animal tree of life
Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., Seaver, E., Rouse, G. W., Obst, M., Edgecombe, G. D., et al. (2008) · Nature · doi:10.1038/nature06614 · Cited by 1,921 · cited 4×
“For example, neither Trichoplax nor representatives of two of the three poriferan classes (31) were included in the study that identified ctenophores as the earliest branching lineage (Figure 1).”
BackgroundInfluentialGenome-scale approaches to resolving incongruence in molecular phylogenies.
Rokas, A., Williams, B. L., King, N., & Carroll, S. B. (2003) · Nature · doi:10.1038/nature02053 · Cited by 1,512
Self-citationThe genome of the social amoeba Dictyostelium discoideum
Eichinger, L., Pachebat, J. A., Glöckner, G., Rajandream, M.-A., Sucgang, R., Berriman, M., Song, J., Olsen, R., Szafranski, K., Xu, Q., et al. (2005) · Nature · doi:10.1038/nature03481 · Cited by 1,351
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans
King, N., Westbrook, M. J., Young, S. L., Kuo, A., Abedin, M., Chapman, J., Fairclough, S., Hellsten, U., Isogai, Y., Letunic, I., et al. (2008) · Nature · doi:10.1038/nature06617 · Cited by 1,139
Self-citationEarly animal evolution: emerging views from comparative biology and geology
Knoll, A. H., & Carroll, S. B. (1999) · Science · doi:10.1126/science.284.5423.2129 · Cited by 821
Life's Solution: Inevitable Humans in a Lonely Universe
Conway Morris, S. (2003) · doi:10.1017/cbo9780511535499 · Cited by 770
The Evolution of Multicellularity: A Minor Major Transition?
Grosberg, R. K., & Strathmann, R. R. (2007) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.36.102403.114735 · Cited by 732
The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?
Douzery, E. J. P., Snell, E. A., Bapteste, E., Delsuc, F., & Philippe, H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403984101 · Cited by 638 · cited 2×
“75 bya (82, 97), a date strikingly contemporaneous with the emergence of the first ancestors of fungi and animals (30, 82).”
BackgroundUnexpected complexity of the Wnt gene family in a sea anemone
Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H. A., Technau, U., von Haeseler, A., Hobmayer, B., Martindale, M. Q., et al. (2005) · Nature · doi:10.1038/nature03158 · Cited by 599
Cited by
The energetics of genome complexity.
Lane, N., & Martin, W. (2010) · Nature · doi:10.1038/nature09486 · Cited by 1,289
An Abundance of Ubiquitously Expressed Genes Revealed by Tissue Transcriptome Sequence Data
Ramsköld, D., Wang, E. T., Burge, C. B., & Sandberg, R. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000598 · Cited by 820
The Origin of Animal Multicellularity and Cell Differentiation
(2017) · doi:10.1016/j.devcel.2017.09.016 · Cited by 419
The Evolution of Extracellular Matrix
Özbek, S., Balasubramanian, P. G., Chiquet-Ehrismann, R., Tucker, R. P., & Adams, J. C. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e10-03-0251 · Cited by 347
The Capsaspora genome reveals a complex unicellular prehistory of animals
Suga, H., Chen, Z., de Mendoza, A., Sebé-Pedrós, A., Brown, M. W., Kramer, E., Carr, M., Kerner, P., Vervoort, M., Sánchez-Pons, N., et al. (2013) · Nature Communications · doi:10.1038/ncomms3325 · Cited by 317
The influence of evolutionary history on human health and disease
Benton, M. L., Abraham, A., LaBella, A. L., Abbot, P., Rokas, A., & Capra, J. A. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-020-00305-9 · Cited by 291
Self-citationGene family innovation, conservation and loss on the animal stem lineage
(2018) · doi:10.7554/elife.34226 · Cited by 226
The Genomic and Cellular Foundations of Animal Origins
Richter, D. J., & King, N. (2013) · Annual Review of Genetics · doi:10.1146/annurev-genet-111212-133456 · Cited by 196
Sebe-Pedros, A., de Mendoza, A., Lang, B. F., Degnan, B. M., & Ruiz-Trillo, I. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msq309 · Cited by 195
Torruella, G., Derelle, R., Paps, J., Lang, B. F., Roger, A. J., Shalchian-Tabrizi, K., & Ruiz-Trillo, I. (2012) · Molecular Biology and Evolution · doi:10.1093/molbev/msr185 · Cited by 169
The Weng'an biota and the Ediacaran radiation of multicellular eukaryotes
Xiao, S., Muscente, A. D., Chen, L., Zhou, C., Schiffbauer, J. D., Wood, A. D., Polys, N. F., & Yuan, X. (2014) · National Science Review · doi:10.1093/nsr/nwu061 · Cited by 172
Connexins: Key Mediators of Endocrine Function
Bosco, D., Haefliger, J.-A., & Meda, P. (2011) · Physiological Reviews · doi:10.1152/physrev.00027.2010 · Cited by 169
Orthology prediction methods: A quality assessment using curated protein families
Trachana, K., Larsson, T. A., Powell, S., Chen, W., Doerks, T., Muller, J., & Bork, P. (2011) · BioEssays · doi:10.1002/bies.201100062 · Cited by 139
The energy expansions of evolution
Judson, O. P. (2017) · Nature Ecology & Evolution · doi:10.1038/s41559-017-0138 · Cited by 118
Alié, A., & Manuel, M. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-34 · Cited by 79
Stevens, A., Hanson, D., Whatmore, A., Destenaves, B., Chatelain, P., & Clayton, P. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-547 · Cited by 65
Sharpe*, S. C., Eme*, L., Brown, M. W., & Roger, A. J. (2015) · Advances in Marine Genomics · doi:10.1007/978-94-017-9642-2_1 · Cited by 49
The Origin of Metazoan Multicellularity: A Potential Microbial Black Swan Event
Ruiz-Trillo, I., Kin, K., & Casacuberta, E. (2023) · Annual Review of Microbiology · doi:10.1146/annurev-micro-032421-120023 · Cited by 36
Origin of Metazoan Developmental Toolkits and Their Expression in the Fossil Record
Tweedt, S. M., & Erwin, D. H. (2015) · Advances in Marine Genomics · doi:10.1007/978-94-017-9642-2_3 · Cited by 27
Role of stellar physics in regulating the critical steps for life
Lingam, M., & Loeb, A. (2019) · International Journal of Astrobiology · doi:10.1017/s1473550419000016 · Cited by 25
Extracellular Matrix Evolution: An Overview
Adams, J. C. (2013) · Biology of Extracellular Matrix · doi:10.1007/978-3-642-36002-2_1 · Cited by 16
Pluralism or unity in biology: could microbes hold the secret to life?
Cleland, C. E. (2013) · Biology & Philosophy · doi:10.1007/s10539-013-9361-7 · Cited by 6
Reduced cell-substrate adhesion formation promotes cell migration in Dictyostelium
Fierro Morales, J. C., A. Nguyen, T., Nepal, S., Redfearn, C., Gale, B. K., Titus, M. A., & Roh-Johnson, M. (2025) · Molecular Biology of the Cell · doi:10.1091/mbc.e25-05-0230 · Cited by 5
Metadata
- Authors
- Rokas, A.
- Venue
- Annual Review of Genetics
- Publisher
- Annual Reviews
- Published
- 2008-12-01
- Volume
- 42
- Issue
- 1
- Pages
- 235-251
- ISSN
- 0066-4197 (ISSN-L)
- 1545-2948
- OpenAlex
- W2097337180
- Cited by
- 311
- References
- 24
- FWCI
- 0.88
- 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.
