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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.
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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
Peterson, K. J., & Eernisse, D. J. (2001) · Evolution & Development · doi:10.1046/j.1525-142x.2001.003003170.x · Cited by 529
The evolution of signalling pathways in animal development
Pires-daSilva, A., & Sommer, R. J. (2003) · Nature Reviews Genetics · doi:10.1038/nrg977 · Cited by 466
Evolution of Key Cell Signaling and Adhesion Protein Families Predates Animal Origins
King, N., Hittinger, C. T., & Carroll, S. B. (2003) · Science · doi:10.1126/science.1083853 · Cited by 424
Peterson, K. J., & Butterfield, N. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503660102 · Cited by 361
Rokas, A., & Carroll, S. B. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040352 · Cited by 315
Self-citationA New Period for the Geologic Time Scale
Knoll, A. H., Walter, M. R., Narbonne, G. M., & Christie-Blick, N. (2004) · Science · doi:10.1126/science.1098803 · Cited by 280
Sponge paraphyly and the origin of Metazoa
Borchiellini, C., Manuel, M., Alivon, E., Boury-Esnault, N., Vacelet, J., & Le Parco, Y. (2001) · Journal of Evolutionary Biology · doi:10.1046/j.1420-9101.2001.00244.x · Cited by 275
Long expected sponges from the Neoproterozoic Ediacara fauna of South Australia
Gehling, J. G., & Rigby, J. K. (1996) · Journal of Paleontology · doi:10.1017/s0022336000023283 · Cited by 256
Mitochondrial genome of Trichoplax adhaerens supports Placozoa as the basal lower metazoan phylum
Dellaporta, S. L., Xu, A., Sagasser, S., Jakob, W., Moreno, M. A., Buss, L. W., & Schierwater, B. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602076103 · Cited by 252
An Ecological Theory for the Sudden Origin of Multicellular Life in the Late Precambrian
Stanley, S. M. (1973) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.70.5.1486 · Cited by 246
A receptor tyrosine kinase from choanoflagellates: Molecular insights into early animal evolution
King, N., & Carroll, S. B. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.261477698 · Cited by 234
A critical reappraisal of the fossil record of the bilaterian phyla
BUDD, G. E., & JENSEN, S. (2000) · Biological Reviews · doi:10.1111/j.1469-185x.1999.tb00046.x · Cited by 145
Fungal fimbriae are composed of collagen
Celerin, M., Ray, J. M., Schisler, N. J., Day, A. W., Stetler‐Stevenson, W. G., & Laudenbach, D. E. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00821.x · Cited by 126
Testing fundamental evolutionary hypotheses
Penny, D., Hendy, M. D., & Poole, A. M. (2003) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(03)00099-7 · Cited by 24
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
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
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