Tradeoff breaking as model of evolutionary transitions in individuality and the limits of the fitness decoupling metaphor

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 an ETI, 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.

Phenotypic plasticity, life cycles, and the evolutionary transition to multicellularity

“…For studying the transition to multicellularity, the importance of the morphological and physiological flexibility of the unicellular ancestor is becoming more and more apparent, for example when studying the complex life cycles of protozoans to infer the last unicellular and last common multicellular ancestor of animals (31) or when comparing experimentally evolved nascent stages of early multicellular life cycles to the highly differentiated life cycles and cells of their closest multicellular relatives. Thus, at least some (if not all) transitions to differentiated multicellularity might have been a rewiring from temporal differentiation of life cycle stages to spatial differentiation in multicellular organisms (35). This poses important questions regarding the ease of such transitions, the ease of reversals to unicellularity, but also regarding our views of the transition to multicellularity (36).…”

Adding causality to the information-theoretic perspective on individuality

“…Black et al (2020) provide several biological situations in which the ecological scaffolding model could be relevant. Note, importantly, that the ecological scaffolding model and, more particularly, the scenario involving niche construction is by no means the only path through which an ETI can occur (Bourrat et al, 2023). I only use this scenario here as an illustration.…”

What Do We Mean by Multicellularity? The Evolutionary Transitions Framework Provides Answers

“…The challenge of identifying criteria for Darwinian individuality has been the subject of much recent discussion. Our aim here is not to review the mechanisms put forward to explain the transition to Darwinian individuality (e.g., Michod, 2005;Godfrey-Smith, 2009;Bourke, 2011;Hammerschmidt et al, 2014;Black et al, 2020;Rose et al, 2020;Bourrat et al, 2021), but rather to remove linguistic ambiguities that may impede fruitful debate.…”