Stability of ecologically scaffolded traits during evolutionary transitions in individuality

Maynard Smith, J. & Szathmáry, E. The Major Transitions in Evolution. (W.H. Freeman, Oxford, 1995).
Google Scholar 
Bourke, A. F. G. Principles of Social Evolution. Oxford Series in Ecology and Evolution. OCLC: ocn700512135, (Oxford University Press, Oxford; New York, 2011).West, S. A., Fisher, R. M., Gardner, A. & Kiers, E. T. Major evolutionary transitions in individuality. Proc. Natl Acad. Sci. 112, 10112–10119 (2015).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Ratcliff, W. C., Herron, M., Conlin, P. L. & Libby, E. Nascent life cycles and the emergence of higher-level individuality. Philos. Trans. R. Soc. B 372, 20160420 (2017).Article 

Google Scholar 
Michod, R. E. On the transfer of fitness from the cell to the multicellularorganism. Biol. Philos. 20, 967–987 (2005).Article 

Google Scholar 
Michod, R. E. Darwinian Dynamics: Evolutionary Transitions in Fitness and Individuality. (Princeton University Press, Princeton, 2000).
Google Scholar 
Buss, L. W. The Evolution of Individuality. (Princeton University Press, Princeton, 1987).
Google Scholar 
Okasha, S. Evolution and the Levels of Selection, 16. (Clarendon Press, Oxford, 2006).van Gestel, J. & Tarnita, C. E. On the origin of biological construction, with a focus on multicellularity. Proc. Natl. Acad. Sci. 201704631. http://www.pnas.org/content/early/2017/09/27/1704631114 (2017).Godfrey-Smith, P. Darwinian Populations and Natural Selection. (Oxford University Press, Oxford, 2009).Hammerschmidt, K., Rose, C. J., Kerr, B. & Rainey, P. B. Life cycles, fitness decoupling and the evolution of multicellularity. Nature 515, 75–79 (2014).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Bonner, J. T. The origins of multicellularity. Integr. Biol.: Issues, N., Rev. 1, 27–36 (1998).Article 

Google Scholar 
Parfrey, L. W. & Lahr, D. J. G. Multicellularity arose several times in the evolution of eukaryotes (Response to DOI 10.1002/bies.201100187). BioEssays 35, 339–347 (2013).Article 
CAS 
PubMed 

Google Scholar 
Herron, M., Conlin, P. L. & Ratcliff, W. The Evolution of Multicellularity. (CRC Press, 2022).Herron, M. D. What are the major transitions? Biol. Philos. 36, 2 (2021).Article 

Google Scholar 
Martin, W. & Russell, M. J. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos. Trans. R. Soc. B: Biol. Sci. 358, 59–85 (2003).Article 
CAS 

Google Scholar 
Archibald, J. M. Endosymbiosis and Eukaryotic Cell Evolution. Curr. Biol. 25, R911–R921 (2015).Article 
CAS 
PubMed 

Google Scholar 
Wilson, E. O. & Hölldobler, B. Eusociality: Origin and consequences. Proc. Natl Acad. Sci. USA 102, 13367–13371 (2005).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Black, A. J., Bourrat, P. & Rainey, P. B. Ecological scaffolding and the evolution of individuality. Nat. Ecol. Evol. 4, 426–436 (2020).Article 
PubMed 

Google Scholar 
Doulcier, G., Lambert, A., De Monte, S. & Rainey, P. B. Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity. eLife 9, e53433 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Bourrat, P. Evolutionary transitions in individuality by endogenization of scaffolded properties. Br. J. Philosophy Sci. https://doi.org/10.1086/719118 (in press).Veit, W. Scaffolding natural selection. Biol. Theory. https://doi.org/10.1007/s13752-021-00387-6 (2021).Neto, C. & Meynell, L. Scaffold: A causal concept for evolutionary explanations. Philosophy Sci. 90, 1224–1233 (2023).Nitschke, M. C., Black, A. J., Bourrat, P. & Rainey, P. B. The effect of bottleneck size on evolution in nested Darwinian populations. J. Theor. Biol., 111414. https://www.sciencedirect.com/science/article/pii/S0022519323000103 (2023).Bourrat, P. et al. Individuality through Ecology: Rethinking the Evolution of Complex Life from an Externalist Perspective (2023). https://osf.io/9h26t.Griesemer, J. & Shavit, A. Scaffolding individuality: coordination, cooperation, collaboration and community. Philos. Trans. R. Soc. B: Biol. Sci. 378, 20210398 (2023).Article 

Google Scholar 
Lewontin, R. C. The units of selection. Annu. Rev. Ecol. Syst. 1, 1–18 (1970).Article 

Google Scholar 
Ratcliff, W. C., Denison, R. F., Borrello, M. & Travisano, M. Experimental evolution of multicellularity. Proc. Natl Acad. Sci. 109, 1595–1600 (2012).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Michod, R. E. & Roze, D. Transitions in individuality. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 264, 853–857 (1997).Article 
ADS 
CAS 

Google Scholar 
Levins, R. Some demographic and genetic consequences of environmental heterogeneity for biological control1. Bull. Entomol. Soc. Am. 15, 237–240 (1969).
Google Scholar 
Kiss, I. Z., Miller, J. C. & Simon, P. L. Mathematics of Epidemics on Networks: From Exact to Approximate Models, vol. 46 of Interdisciplinary Applied Mathematics (Springer International Publishing, Cham, 2017) http://link.springer.com/10.1007/978-3-319-50806-1.Nowak, M. A. & May, R. M. Evolutionary games and spatial chaos. Nature 359, 826–829 (1992).Article 
ADS 

Google Scholar 
Hogeweg, P. Multilevel Processes in Evolution and Development: Computational Models and Biological Insights. In Biological Evolution and Statistical Physics (eds. Lässig, M. & Valleriani, A.) 217–239 (Springer, Berlin, Heidelberg, 2002). https://doi.org/10.1007/3-540-45692-9_12.Geritz, S. A. H., Kisdi, E., Meszéna, G. & Metz, Ja. J. Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evolut. Ecol. 12, 35–57 (1998).Article 

Google Scholar 
Miele, L. & De Monte, S. Aggregative cycles evolve as a solution to conflicts in social investment. PLOS Comput. Biol. 17, e1008617 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Doulcier, G., Hammerschmidt, K. & Bourrat, P. Group Transformation: Life History Trade-Offs, Division of Labor, and Evolutionary Transitions in Individuality. In The Evolution of Multicellularity (eds. Herron, M. D., Conlin, P. L. & Ratcliff, W. C.) 227–246 (CRC Press, Roca Baton, FL, 2022).Beisner, B., Haydon, D. & Cuddington, K. Alternative stable states in ecology. Front. Ecol. Environ. 1, 376–382 (2003).Article 

Google Scholar 
Noori, H. R. Examples of Hysteresis Phenomena in Biology. In Hysteresis Phenomena in Biology (ed. Noori, H. R.) SpringerBriefs in Applied Sciences and Technology, 35–45 (Springer, Berlin, Heidelberg, 2014). https://doi.org/10.1007/978-3-642-38218-5_4.Michod, R. E. The group covariance effect and fitness trade-offs during evolutionary transitions in individuality. Proc. Natl Acad. Sci. 103, 9113–9117 (2006).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Herron, M. D. & Ratcliff, W. C. Trait Heritability in Major Transitions. bioRxiv041830. http://biorxiv.org/content/early/2016/02/29/041830 (2016).Metz, J. A. J., Nisbet, R. M. & Geritz, S. A. H. How should we define ‘fitness’ for general ecological scenarios? Trends Ecol. Evol. 7, 198–202 (1992).Article 
CAS 
PubMed 

Google Scholar 
Pepper, J. W. & Herron, M. D. Does biology need an organism concept? Biol. Rev. 83, 621–627 (2008).Article 
PubMed 

Google Scholar 
Calcott, B. & Sterelny, K. The Major Transitions in Evolution Revisited. (MIT Press, Cambridge, MA, 2011).Bouchard, F. & Huneman, P. From Groups to Individuals: Evolution and Emerging Individuality. (MIT Press, Cambridge, MA, 2013).Book 

Google Scholar 
Clarke, E. Origins of evolutionary transitions. J. Biosci. 39, 303–317 (2014).Article 
PubMed 

Google Scholar 
Guay, A. & Pradeu, T. (eds) Individuals Across the Sciences. (Oxford University Press, 2015).Lidgard, S. & Nyhart, L. K. The Work of Biological Individuality: Concepts and Contexts. In Biological Individuality: Integrating Scientific, Philosophical, and Historical Perspectives (eds. Lidgard, S. & Nyhart, L. K.) 17–62 (University of Chicago Press, Chicago ; London, 2017).Bourrat, P. A coarse-graining account of individuality: how the emergence of individuals represents a summary of lower-level evolutionary processes. Biol. Philos. 38, 33 (2023).Article 
PubMed 
PubMed Central 

Google Scholar 
Godfrey-Smith, P. Varieties of population structure and the levels of selection. Br. J. Philos. Sci. 59, 25–50 (2008).Article 

Google Scholar 
Bourrat, P. Facts, Conventions, and the Levels of Selection. (Cambridge University Press, 2021). https://www.cambridge.org/core/elements/facts-conventions-and-the-levels-of-selection/8EAF88974A3BE92761217A2EC6AB4634.Bourrat, P. Transitions in evolution: a formal analysis. Synthese 198, 3699–3731 (2021).Article 
MathSciNet 

Google Scholar 
Libby, E. & Ratcliff, W. C. Ratcheting the evolution of multicellularity. Science 346, 426–427 (2014).Article 
ADS 
CAS 
PubMed 

Google Scholar 
Libby, E., Conlin, P. L., Kerr, B. & Ratcliff, W. C. Stabilizing multicellularity through ratcheting. Philos. Trans. R. Soc. B: Biol. Sci. 371, 20150444 (2016).Article 

Google Scholar 
Clarke, E. The multiple realizability of biological individuals. J. Philos. 110, 413–435 (2013).Article 

Google Scholar 
Tarnita, C. E., Taubes, C. H. & Nowak, M. A. Evolutionary construction by staying together and coming together. J. Theor. Biol. 320, 10–22 (2013).Article 
ADS 
MathSciNet 
PubMed 

Google Scholar 
Pichugin, Y., Peña, J., Rainey, P. B. & Traulsen, A. Fragmentation modes and the evolution of life cycles. PLOS Comput. Biol. 13, e1005860 (2017).Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 
Bozdag, G. O. et al. De novo evolution of macroscopic multicellularity. Nature 617, 747–754 (2023).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Ratcliff, W. C. et al. Experimental evolution of an alternating uni- and multicellular life cycle in Chlamydomonas reinhardtii. Nat. Commun. 4, 2742 (2013).Article 
ADS 
PubMed 

Google Scholar 
Tang, S., Pichugin, Y. & Hammerschmidt, K. An environmentally induced multicellular life cycle of a unicellular cyanobacterium. Curr. Biol.: CB 33, 764–769.e5 (2023).Article 
PubMed 

Google Scholar 
Savill, N. J. & Hogeweg, P. Modelling morphogenesis: from single cells to crawling slugs. J. Theor. Biol. 184, 229–235 (1997).Article 
ADS 
PubMed 

Google Scholar 
Garcia, T., Doulcier, G. & De Monte, S. The evolution of adhesiveness as a social adaptation. eLife, e08595 (2015).Vroomans, R. M. A., Hogeweg, P. & ten Tusscher, K. H. W. J. Segment-specific adhesion as a driver of convergent extension. PLoS Comput. Biol. 11, e1004092 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Colizzi, E. S., Vroomans, R. M. & Merks, R. M. Evolution of multicellularity by collective integration of spatial information. eLife 9, e56349 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Pfeiffer, T. & Bonhoeffer, S. An evolutionary scenario for the transition to undifferentiated multicellularity. Proc. Natl Acad. Sci. 100, 1095–1098 (2003).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Hermsen, R. Emergent multilevel selection in a simple spatial model of the evolution of altruism. PLOS Comput. Biol. 18, e1010612 (2022).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Takeuchi, N. & Hogeweg, P. Multilevel selection in models of prebiotic evolution II: a direct comparison of compartmentalization and spatial self-organization. PLOS Comput. Biol. 5, e1000542 (2009).Article 
ADS 
MathSciNet 
PubMed 
PubMed Central 

Google Scholar 
Mustonen, V. & Lässig, M. From fitness landscapes to seascapes: non-equilibrium dynamics of selection and adaptation. Trends Genet. 25, 111–119 (2009).Article 
CAS 
PubMed 

Google Scholar 
Lyons, N. A. & Kolter, R. On the evolution of bacterial multicellularity. Curr. Opin. Microbiol. 24, 21–28 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Bonforti, A. & Solé, R. Unicellular-multicellular evolutionary branching driven by resource limitations. J. R. Soc. Interface 19, 20220018 (2022).Article 
PubMed 
PubMed Central 

Google Scholar 
Szathmáry, E. Modeling the origin of cells. Trends Genet. 39, 719–720 (2023).Article 
PubMed 

Google Scholar 
Babajanyan, S. G. et al. Coevolution of reproducers and replicators at the origin of life and the conditions for the origin of genomes. Proc. Natl Acad. Sci. 120, e2301522120 (2023).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Rainey, P. B. & Kerr, B. Cheats as first propagules: A new hypothesis for the evolution of individuality during the transition from single cells to multicellularity. BioEssays 32, 872–880 (2010).Article 
PubMed 

Google Scholar 
Carr, G. M. & Macdonald, D. W. The sociality of solitary foragers: a model based on resource dispersion. Anim. Behav. 34, 1540–1549 (1986).Article 

Google Scholar 
Johnson, D. D., Kays, R., Blackwell, P. G. & Macdonald, D. W. Does the resource dispersion hypothesis explain group living? Trends Ecol. Evol. 17, 563–570 (2002).Article 

Google Scholar 
Kimura, M. & Maruyama, T. Pattern of neutral polymorphism in a geographically structured population. Genetical Res. 18, 125–131 (1971).Article 
CAS 

Google Scholar 
Williams, G. C. Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. (Princeton University Press, Princeton, 1966).
Google Scholar 
Damuth, J. & Heisler, I. L. Alternative formulations of multilevel selection. Biol. Philos. 3, 407–430 (1988).Article 

Google Scholar 
Brandon, R. N. Adaptation and Environment. (Princeton University Press, Princeton, NJ, 1990).
Google Scholar 
Sober, E. The Nature of Selection. (MIT Press, Cambridge, MA, 1984).Wimsatt, W. C. Re-Engineering Philosophy for Limited Beings: Piecewise Approximations to Reality. (Harvard University Press, Cambridge, Mass, 2007).Book 

Google Scholar 
Shelton, D. E. & Michod, R. E. Group selection and group adaptation during a major evolutionary transition: insights from the evolution of multicellularity in the volvocine algae. Biol. Theory 9, 452–469 (2014).Article 

Google Scholar 
Shelton, D. E. & Michod, R. E. Group and individual selection during evolutionary transitions in individuality: meanings and partitions. Philos. Trans. R. Soc. B: Biol. Sci. 375, 20190364 (2020).Article 

Google Scholar 
Bijma, P. The quantitative genetics of indirect genetic effects: a selective review of modelling issues. Heredity 112, 61–69 (2014).Article 
CAS 
PubMed 

Google Scholar 
Walsh, B. & Lynch, M. Evolution and Selection of Quantitative Traits. (Oxford University Press, New York, 2018).Book 

Google Scholar 
Bourrat, P. Multilevel selection 1, multilevel selection 2, and the Price equation: a reappraisal. Synthese 202, 72 (2023).Article 
MathSciNet 

Google Scholar 
Wilson, D. S. & Sober, E. Reintroducing group selection to the human behavioral sciences. Behav. Brain Sci. 17, 585–608 (1994).Article 

Google Scholar 
Santelices, B. How many kinds of individual are there? Trends Ecol. Evol. 14, 152–155 (1999).Article 
CAS 
PubMed 

Google Scholar 
Clarke, E. The problem of biological individuality. Biol. Theory 5, 312–325 (2010).Article 

Google Scholar 
Simpson, C. How many levels are there? How insights from evolutionary transitions in individuality help measure the hierarchical complexity of life. In The Major Transitions in Evolution Revisited (The MIT Press, 2011).Michod, R. E. Cooperation and conflict in the evolution of individuality. II. Conflict mediation. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 263, 813–822 (1996).Article 
ADS 
CAS 

Google Scholar 
Bourrat, P., Doulcier, G., Rose, C. J., Rainey, P. B. & Hammerschmidt, K. Tradeoff breaking as model of evolutionary transitions in individuality and the limits of the fitness-decoupling metaphor. eLife 11, e73715 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Swenson, W., Wilson, D. S. & Elias, R. Artificial ecosystem selection. Proc. Natl Acad. Sci. 97, 9110–9114 (2000).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Panke-Buisse, K., Poole, A. C., Goodrich, J. K., Ley, R. E. & Kao-Kniffin, J. Selection on soil microbiomes reveals reproducible impacts on plant function. ISME J. 9, 980–989 (2015).Article 
CAS 
PubMed 

Google Scholar 
Xie, L., Yuan, A. E. & Shou, W. Simulations reveal challenges to artificial community selection and possible strategies for success. PLOS Biol. 17, e3000295 (2019).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Rose, C. J., Hammerschmidt, K., Pichugin, Y. & Rainey, P. B. Meta-population structure and the evolutionary transition to multicellularity. Ecol. Lett. 23, 1380–1390 (2020).Article 
PubMed 

Google Scholar 
Arias-Sánchez, F. I., Vessman, B. & Mitri, S. Artificially selecting microbial communities: If we can breed dogs, why not microbiomes? PLOS Biol. 17, e3000356 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Russell, M. J. & Hall, A. J. The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J. Geol. Soc. 154, 377–402 (1997).Article 
ADS 
CAS 

Google Scholar 
Russell, M. J., Daniel, R. M., Hall, A. J. & Sherringham, J. A. A hydrothermally precipitated catalytic iron sulphide membrane as a first step toward life. J. Mol. Evol. 39, 231–243 (1994).Article 
ADS 
CAS 

Google Scholar 
von der Dunk, S. H. A., Snel, B. & Hogeweg, P. Evolution of complex regulation for cell-cycle control. Genome Biol. Evol. 14, evac056 (2022).Article 
PubMed 
PubMed Central 

Google Scholar 
Harris, C. R. et al. Array programming with NumPy. Nature 585, 357–362 (2020).Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Virtanen, P. et al. SciPy 1.0: fundamental algorithms for scientific computing in Python. Nat. Methods 17, 261–272 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Hunter, J. D. Matplotlib: A 2D graphics environment. Comput. Sci. Eng. 9, 90–95 (2007).Article 

Google Scholar 

Hot Topics

Related Articles