Tradeoff breaking as a model of evolutionary transitions in individuality and 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. Extending and unifying results from the literature, we show that fitness of particles and collectives can never decouple because calculations of particle and collective fitness performed over appropriate and equivalent time intervals are necessarily the same provided the population reaches a stable collective size distribution. By way of solution, we draw attention to the value of mechanistic approaches that emphasise traits, and tradeoffs among traits, as opposed to fitness. 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 the rupture of such tradeoffs. Thus, when observed in the context of ETIs, tradeoff-breaking events stand as a useful marker for these transitions.

Reproductive restraint to avoid the costs of reproductive conflict in a cooperatively breeding mammal

“…The reduction in internal conflict among related males in banded mongoose groups is consistent with recent ideas suggesting a key step in evolutionary transitions to higher levels of social organisation is the breaking of life history tradeoffs (i.e. major evolutionary transitions) [96]. Kin selection may favour low condition males to remain inactive in order to allow higher condition males to reproduce who face a weakened trade-off between reproduction and survival.…”

Adaptation in the face of internal conflict: the paradox of the organism revisited

“…(2) Enforcement of cooperation Different types of organisms have come into being via evolutionary transitions in individuality (Maynard Smith & Szathm ary, 1995;Bourke, 2011;West et al, 2015). These are fundamental changes in the social organisation of biological entities, whereby lower-level units (particles) become organised into higher-level ones (collectives), typically associated with the transfer of fitness from particles to collectives (Michod, 1999(Michod, , 2007Clarke, 2014; but see Bourrat et al, 2022). For example, eukaryotes represent collectives of genomes, multicellular organisms represent collectives of cells, and all organisms can be regarded as collectives of genes that have become organised into genomes.…”

“…Within the lifespan of the organism, we may thus talk of cancer cells being selected for and causing change within the developing body . But these changes are wiped out in the next generation of organisms because, in general, all of the ‘evolution’ that cancer causes takes place in the ephemeral soma (Gardner, 2014; Bourrat et al ., 2022). This is not the sort of selection within organisms that could ever lead to the evolution of increased cancer over evolutionary time.…”

Quantifying internal conflicts and their threats to organismal form and fitness

“…Looked at another way, the Paradox asks why the major transitions in individuality do not seem to go in reverse. Organisms are collectives made of parts (e.g., genes, genomes, and cells) that had had their own purposes earlier in evolutionary history but that can now function only as part of higher levels of individuality (West et al, 2015;Bourrat et al, 2022;Bourke, 2023;Doulcier et al, 2023). These 'collective agents' clearly harbor internal conflicts over the direction of the organism, but why do they not get out of hand?…”