Stability of Ecologically Scaffolded Traits During Evolutionary Transitions in Individuality

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Abstract

Evolutionary transitions in individuality (ETIs), such as the emergence of multicellularity, are events in the history of life during which entities at one level of organisation (particles) form collective-level entities that subsequently become individuals in their own right. Recent empirical and theoretical studies advocate the importance of an externally imposed meta-population structure or “ecological scaffold” for the emergence of new levels of individuality. Such a scaffold enables survival and reproduction at the collective level and thus the possibility of selection for beneficial traits on that level. However, a long-standing difficulty for the ecological scaffolding approach has been its inability to adequately explain how collective-level trait values that evolved under scaffolding conditions can be retained once these conditions are lifted. We call this difficulty “the problem of endogenisation.” Here, we derive general conditions for the possibility of endogenisation. Key to endogenisation is the existence of a fitness valley that can be circumvented when scaffolding occurs. Using a stochastic meta-population model, we implement two versions of ecological scaffolding (one temporal and one spatial) and study subsequent evolutionary trajectories using the modelling techniques of adaptive dynamics. Our analysis yields several important results. The temporal model reveals that only collective traits based on particle-particle interactions can be endogenised when a temporary scaffold is applied to the entire population. The spatial model shows that, given the presence of an environmental gradient of externally imposed meta-population structure, ecological scaffolding can only occur in a limited “Goldilocks” zone of the environment. Further, if endogenisation conditions are also fulfilled, scaffolded collectives can colonise non-scaffolding areas of the environment. We conjecture that Goldilocks zones could act as initiators of ETIs and help explain the near ubiquity of collective-level individuality even if the conditions that promote it prove to be rare.

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