Stabilizing multicellularity through ratcheting
Open accessAbstract
The evolutionary transition to multicellularity probably began with the formation of simple undifferentiated cellular groups. Such groups evolve readily in diverse lineages of extant unicellular taxa, suggesting that there are few genetic barriers to this first key step. This may act as a double-edged sword: labile transitions between unicellular and multicellular states may facilitate the evolution of simple multicellularity, but reversion to a unicellular state may inhibit the evolution of increased complexity. In this paper, we examine how multicellular adaptations can act as evolutionary 'ratchets', limiting the potential for reversion to unicellularity. We consider a nascent multicellular lineage growing in an environment that varies between favouring multicellularity and favouring unicellularity. The first type of ratcheting mutations increase cell-level fitness in a multicellular context but are costly in a single-celled context, reducing the fitness of revertants. The second type of ratcheting mutations directly decrease the probability that a mutation will result in reversion (either as a pleiotropic consequence or via direct modification of switch rates). We show that both types of ratcheting mutations act to stabilize the multicellular state. We also identify synergistic effects between the two types of ratcheting mutations in which the presence of one creates the selective conditions favouring the other. Ratcheting mutations may play a key role in diverse evolutionary transitions in individuality, sustaining selection on the new higher-level organism by constraining evolutionary reversion.This article is part of the themed issue 'The major synthetic evolutionary transitions'.
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
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.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Ratcheting processes, where cells acquire traits that commit them to a group lifestyle, stabilize the group and may serve as a universal mechanism that propels multicellular complexity.
“This is enabled by ‘ratcheting’ processes where cells acquire traits that commit them to a group lifestyle. This stabilizes the group and may serve as a universal mechanism that propels multicellular complexity [201,202].”
From Fundamental constraints to the logic of living systems (2024) · cites this paper as [201]
The Discussion (page not provided) says ratcheting traits can stabilize multicellularity against reversion and may facilitate increased complexity. It does not establish a universal mechanism: it describes ratcheting as a possible stepping stone and notes that such traits would be detrimental in life cycles that require switching between unicellular and multicellular forms. (LLM, conf=0.86)
Experimental — accuracy not yet measuredOne solution to stabilizing MC against cheaters is the evolution of traits that increase cell-level fitness in a group context but come at a cost to free-living fitness.
“One solution to stabilizing MC against cheaters is the evolution of traits that increase cell-level fitness in a group context but come at a cost to free-living fitness.”
From Fundamental constraints to the logic of living systems (2024) · cites this paper as [201]
The Introduction and Discussion describe traits that improve fitness in a multicellular context while reducing it in a unicellular context, thereby stabilizing multicellularity against reversion. The paper distinguishes reversion to unicellularity from conflict among competing cells within a group; it does not establish this mechanism as a solution specifically against cheaters. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Exact stochastic simulation of coupled chemical reactions
Gillespie, D. T. (1977) · The Journal of Physical Chemistry · doi:10.1021/j100540a008 · Cited by 9,969 · see citing works
The fate of competing beneficial mutations in an asexual population
Gerrish, P. J., & Lenski, R. E. (1998) · Genetica · doi:10.1023/a:1017067816551 · Cited by 783 · see citing works
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 · see citing works
The Genome of M. acetivorans Reveals Extensive Metabolic and Physiological DiversityPreprint
Galagan, J. E., Nusbaum, C., Roy, A., Endrizzi, M. G., Macdonald, P., FitzHugh, W., Calvo, S., Engels, R., Smirnov, S., Atnoor, D., et al. (2002) · Genome Research · doi:10.1101/gr.223902 · Cited by 625 · see citing works
Experimental evolution of multicellularity
Ratcliff, W. C., Denison, R. F., Borrello, M., & Travisano, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1115323109 · Cited by 570 · see citing works
Self-citationEvolution of cooperation and conflict in experimental bacterial populations
Rainey, P. B., & Rainey, K. (2003) · Nature · doi:10.1038/nature01906 · Cited by 568 · see citing works
The Unicellular Ancestry of Animal Development
King, N. (2004) · Developmental Cell · doi:10.1016/j.devcel.2004.08.010 · Cited by 482 · see citing works
The origins of multicellularity
Bonner, J. T. (1998) · Integrative Biology Issues News and Reviews · doi:10.1002/(sici)1520-6602(1998)1:1 · Cited by 455 · see citing works
FLO1 Is a Variable Green Beard Gene that Drives Biofilm-like Cooperation in Budding Yeast
Smukalla, S. M., Caldara, M., Pochet, N. L. M. M., Beauvais, A., Guadagnini, S., Chen, Y., Vinces, M. D., Jansen, A., Prévost, M. C., Latgé, J., et al. (2008) · Cell · doi:10.1016/j.cell.2008.09.037 · Cited by 453 · see citing works
A twelve-step program for evolving multicellularity and a division of labor
Kirk, D. L. (2005) · BioEssays · doi:10.1002/bies.20197 · Cited by 345 · see citing works
Alternative formulations of multilevel selection
Damuth, J. D., & Heisler, I. L. (1988) · Biology & Philosophy · doi:10.1007/bf00647962 · Cited by 326 · see citing works
Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago
Albani, A. E., Bengtson, S., Canfield, D. E., Bekker, A., Macchiarelli, R., Mazurier, A., Hammarlund, E. U., Boulvais, P., Dupuy, J.-J., Fontaine, C., et al. (2010) · Nature · doi:10.1038/nature09166 · Cited by 315 · see citing works
Single-Gene Greenbeard Effects in the Social Amoeba Dictyostelium discoideum
Queller, D. C., Ponte, E., Bozzaro, S., & Strassmann, J. E. (2003) · Science · doi:10.1126/science.1077742 · Cited by 305 · see citing works
Triassic origin and early radiation of multicellular volvocine algae
Herron, M. D., Hackett, J. D., Aylward, F. O., & Michod, R. E. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811205106 · Cited by 285 · see citing works
Reduction of adaptive genetic diversity radically alters eco‐evolutionary community dynamics
Becks, L., Ellner, S. P., Jones, L., & Hairston, N. G. (2010) · Ecology Letters · doi:10.1111/j.1461-0248.2010.01490.x · Cited by 282 · see citing works
Spiers, A. J., Kahn, S. G., Bohannon, J., Travisano, M., & Rainey, P. B. (2002) · Genetics · doi:10.1093/genetics/161.1.33 · Cited by 281 · see citing works
Phagotrophy by a flagellate selects for colonial prey: A possible origin of multicellularity
Boraas, M. E., Seale, D. B., & Boxhorn, J. E. (1998) · Evolutionary Ecology · doi:10.1023/a:1006527528063 · Cited by 250 · see citing works
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 · see citing works
Sucrose Utilization in Budding Yeast as a Model for the Origin of Undifferentiated Multicellularity
Koschwanez, J. H., Foster, K. R., & Murray, A. W. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001122 · Cited by 243 · see citing works
Lineage selection and the evolution of multistage carcinogenesis
Nunney, L. (1999) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1999.0664 · Cited by 208 · see citing works
Origins of multicellular evolvability in snowflake yeast
Ratcliff, W. C., Fankhauser, J. D., Rogers, D. W., Greig, D., & Travisano, M. (2015) · Nature Communications · doi:10.1038/ncomms7102 · Cited by 203 · see citing works
Self-citationAn evolutionary scenario for the transition to undifferentiated multicellularity
Pfeiffer, T., & Bonhoeffer, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0335420100 · Cited by 183 · see citing works
Ratcliff, W. C., Herron, M. D., Howell, K., Pentz, J. T., Rosenzweig, F., & Travisano, M. (2013) · Nature Communications · doi:10.1038/ncomms3742 · Cited by 174 · see citing works
Self-citationGrosberg, R. K., & Strathmann, R. R. (1998) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(97)01313-x · Cited by 154 · see citing works
McDonald, M. J., Gehrig, S. M., Meintjes, P., Zhang, X., & Rainey, P. B. (2009) · Genetics · doi:10.1534/genetics.109.107110 · Cited by 150 · see citing works
On the Reorganization of Fitness During Evolutionary Transitions in Individuality
Michod, R. E. (2003) · Integrative and Comparative Biology · doi:10.1093/icb/43.1.64 · Cited by 149 · see citing works
Multilevel Selection and the Major Transitions in Evolution
Okasha, S. (2005) · Philosophy of Science · doi:10.1086/508102 · Cited by 144 · see citing works
Improved use of a public good selects for the evolution of undifferentiated multicellularity
Koschwanez, J. H., Foster, K. R., & Murray, A. W. (2013) · eLife · doi:10.7554/elife.00367 · Cited by 136 · see citing works
Cooperation and conflict in the evolution of individuality. II. Conflict mediation
Michod, R. E. (1996) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1996.0121 · Cited by 124 · see citing works
How cellular slime molds evade nematodes.
Kessin, R. H., Gundersen, G. G., Zaydfudim, V. M., & Grimson, M. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.10.4857 · Cited by 88 · see citing works
Cheater-resistance is not futile
Khare, A., Santorelli, L. A., Strassmann, J. E., Queller, D. C., Kuspa, A., & Shaulsky, G. (2009) · Nature · doi:10.1038/nature08472 · Cited by 86 · see citing works
A conceptual framework for the evolutionary origins of multicellularity
Libby, E., & B Rainey, P. (2013) · Physical Biology · doi:10.1088/1478-3975/10/3/035001 · Cited by 81 · see citing works
Self-citationRatcheting the evolution of multicellularity
Libby, E., & Ratcliff, W. C. (2014) · Science · doi:10.1126/science.1262053 · Cited by 72 · see citing works
Self-citationExperimental evolution of selfish policing in social bacteria
Manhes, P., & Velicer, G. J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1014695108 · Cited by 68 · see citing works
Roze, D., & Michod, R. E. (2001) · The American Naturalist · doi:10.1086/323590 · Cited by 67 · see citing works
Geometry Shapes Evolution of Early Multicellularity
Libby, E., Ratcliff, W. C., Travisano, M., & Kerr, B. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003803 · Cited by 58 · see citing works
Self-citationShelton, D. E., & Michod, R. E. (2014) · Biological Theory · doi:10.1007/s13752-014-0159-x · Cited by 49 · see citing works
Mutation load under vegetative reproduction and cytoplasmic inheritance.
Kondrashov, A. S. (1994) · Genetics · doi:10.1093/genetics/137.1.311 · Cited by 45 · see citing works
Nutrient shielding in clusters of cells
Lavrentovich, M. O., Koschwanez, J. H., & Nelson, D. R. (2013) · Physical Review E · doi:10.1103/physreve.87.062703 · Cited by 37 · see citing works
Cooperation, clumping and the evolution of multicellularity
Biernaskie, J. M., & West, S. A. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.1075 · Cited by 33 · see citing works
A model for the origin of group reproduction during the evolutionary transition to multicellularity
Maliet, O., Shelton, D. E., & Michod, R. E. (2015) · Biology Letters · doi:10.1098/rsbl.2015.0157 · Cited by 33 · see citing works
Yokota, K., & Sterner, R. W. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2010.1459 · Cited by 26 · see citing works
Evolution of cyanobacterial morphotypes: Taxa required for improved phylogenomic approaches.
Schirrmeister, B. E., Anisimova, M. O., Antonelli, A., & Bagheri, H. C. (2011) · PubMed Central · doi:10.4161/cib.16183 · Cited by 22 · see citing works
Collins, A. G. (2000) · doi:10.1666/0094-8373(2000)026
Simpson, C. (2011) · The Major Transitions in Evolution Revisited · doi:10.7551/mitpress/9780262015240.003.0011
Trade-offs Drive the Evolution of Increased Complexity in Nascent Multicellular Digital Organisms
Conlin, P. L., & Ratcliff, W. C. (2016) · Multicellularity · doi:10.7551/mitpress/10525.003.0014
Self-citation
Flagged first, then by citations
Research works printed but not linked: 5
- [1]Buss LW 1987 The evolution of individuality. Princeton, NJ: Princeton University Press.
- [2]Smith JM, Szathmáry E 1995 The major transitions in evolution. Oxford, UK: Oxford University Press.
- [3]Michod RE, Roze D 1999 Cooperation and conflict in the evolution of individuality. III. Transitions in the unit of fitness. In Mathematical and computational biology: computational morphogenesis, hierarchical complexity, and digital evolution (ed. Nehaniv CL), pp. 47– 92. Providence, RI: American Mathematical Society.
- [13]Bonner JT 2001 First signals: the evolution of multicellular development. Princeton, NJ: Princeton University Press.
- [50]Godfrey-Smith P 2009 Darwinian populations and natural selection. New York, NY: Oxford University Press.
Cited by
Sorted by citations
Fundamental constraints to the logic of living systems
Solé, R., Kempes, C. P., Corominas-Murtra, B., De Domenico, M., Kolchinsky, A., Lachmann, M., Libby, E., Saavedra, S., Smith, E., & Wolpert, D. (2024) · Interface Focus · doi:10.1098/rsfs.2024.0010 · Cited by 34 · see citing works
Self-citation
- Authors
- Libby, E., Conlin, P. L., Kerr, B., & Ratcliff, W. C.
- Affiliations
- Santa Fe Institute (US)
- University of Washington (US)
- Department of Biology and BEACON Center for the Study of Evolution in Action, University of Washington, Seattle, WA 98195, USA
- Georgia Institute of Technology (US)
- Corresponding author
- Libby, Eric
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2016-08-19
- Volume
- 371
- Issue
- 1701
- Pages
- 20150444
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC4958938
- OpenAlex
- W2496969863
- Cited by
- 58
- References
- 46
- Citations by year
- 2025: 15 · 2024: 9 · 2023: 4 · 2022: 3 · 2021: 7 · 2020: 4 · 2019: 6 · 2018: 6 · 2017: 3 · 2016: 1
- FWCI
- 4.31
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (DBI-0939454, DGE-1256082)
- National Aeronautics and Space Administration (NNX15AR33G)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Social Sciences › Sociology and Political Science › Evolutionary Game Theory and Cooperation
- Social Sciences › Arts and Humanities › History and Philosophy of Science › Philosophy and History of Science
- Keywords
- evolution of multicellularity, evolutionary transitions, individuality, pleiotropy, environmental variability
- MeSH terms
- Adaptation, Biological, Biological Evolution, Models, Genetic, Selection, Genetic, Eukaryota
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