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Beyond Fitness Decoupling: Tradeoff-breaking during Evolutionary Transitions in Individuality

View ORCID ProfilePierrick Bourrat, View ORCID ProfileGuilhem Doulcier, View ORCID ProfileCaroline J. Rose, View ORCID ProfilePaul B. Rainey, View ORCID ProfileKatrin Hammerschmidt
doi: https://doi.org/10.1101/2021.09.01.458526
Pierrick Bourrat
1Philosophy Department, Macquarie University, New South Wales 2109, Australia
2Department of Philosophy & Charles Perkins Centre, The University of Sydney, New South Wales 2006, Australia
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  • For correspondence: p.bourrat@gmail.com guihem.doulcier@normalesup.org katrinhammerschmidt@googlemail.com
Guilhem Doulcier
2Department of Philosophy & Charles Perkins Centre, The University of Sydney, New South Wales 2006, Australia
3Laboratory of Biophysics and Evolution, Chemistry, Biology and Innovation (CBI) UMR8231, ESPCI Paris, CNRS, PSL Research University, 10 rue Vauquelin, Paris, France
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  • For correspondence: p.bourrat@gmail.com guihem.doulcier@normalesup.org katrinhammerschmidt@googlemail.com
Caroline J. Rose
4Centre d’Écologie Fonctionnelle et Évolutive (CEFE), CNRS, Montpellier, France
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Paul B. Rainey
3Laboratory of Biophysics and Evolution, Chemistry, Biology and Innovation (CBI) UMR8231, ESPCI Paris, CNRS, PSL Research University, 10 rue Vauquelin, Paris, France
5Max Planck Institute for Evolutionary Biology, Plön, Germany
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Katrin Hammerschmidt
6Institute of Microbiology, Kiel University, Kiel, Germany
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  • For correspondence: p.bourrat@gmail.com guihem.doulcier@normalesup.org katrinhammerschmidt@googlemail.com
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Abstract

Evolutionary transitions in individuality (ETIs) involve the formation of Darwinian collectives from Darwinian particles. The transition from cells to multicellular life is a prime example. During anETI, collectives become units of selection in their own right. However, the underlying processes are poorly understood. One observation used to identify the completion of an ETI is an increase in collective-level performance accompanied by a decrease in particle-level performance, for example, measured by growth rate. This seemingly counterintuitive dynamic has been referred to as “fitness decoupling” and has been used to interpret both models and experimental data. Using a mathematical approach we show this concept to be problematic in that the fitness of particles and collectives can never decouple: calculations of particle and collective fitness performed over appropriate and equivalent time intervals are necessarily the same. By way of solution, we draw attention to the value of mechanistic approaches that emphasise traits as opposed to fitness and tradeoffs among traits. This trait-based approach is sufficient to capture dynamics that underpin evolutionary transitions. In addition, drawing upon both experimental and theoretical studies, we show that while early stages of transitions might often involve tradeoffs among particle traits, later—and critical—stages are likely to involve rupture of such tradeoffs. Tradeoff-breaking thus stands as a useful marker for ETIs.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://doi.org/10.5281/zenodo.5352208

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted September 02, 2021.
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Beyond Fitness Decoupling: Tradeoff-breaking during Evolutionary Transitions in Individuality
Pierrick Bourrat, Guilhem Doulcier, Caroline J. Rose, Paul B. Rainey, Katrin Hammerschmidt
bioRxiv 2021.09.01.458526; doi: https://doi.org/10.1101/2021.09.01.458526
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Beyond Fitness Decoupling: Tradeoff-breaking during Evolutionary Transitions in Individuality
Pierrick Bourrat, Guilhem Doulcier, Caroline J. Rose, Paul B. Rainey, Katrin Hammerschmidt
bioRxiv 2021.09.01.458526; doi: https://doi.org/10.1101/2021.09.01.458526

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