Abstract

Evolution is often conceived as changes in the properties of a population over generations. Does this notion exhaust the possible dynamics of evolution? Life is hierarchically organized, and evolution can operate at multiple levels with conflicting tendencies. Using a minimal model of such conflicting multilevel evolution, we demonstrate the possibility of a novel mode of evolution that challenges the above notion: individuals ceaselessly modify their genetically inherited phenotype and fitness along their lines of descent, without involving apparent changes in the properties of the population. The model assumes a population of primitive cells (protocells, for short), each containing a population of replicating catalytic molecules. Protocells are selected towards maximizing the catalytic activity of internal molecules, whereas molecules tend to evolve towards minimizing it in order to maximize their relative fitness within a protocell. These conflicting evolutionary tendencies at different levels and genetic drift drive the lineages of protocells to oscillate endlessly between high and low intracellular catalytic activity, i.e. high and low fitness, along their lines of descent. This oscillation, however, occurs independently in different lineages, so that the population as a whole appears stationary. Therefore, ongoing evolution can be hidden behind an apparently stationary population owing to conflicting multilevel evolution.

Highlights

  • Evolution is often conceived as changes in the properties of a population over generations [1,2,3]

  • This notion is likely to be valid under many circumstances, does it exhaust the possible dynamics of evolution?

  • Similar examples abound throughout the biological hierarchy: the evolution of eukaryotes and selfish organelles [9,10], the evolution of multicellular organisms and cancer cells [11], and the evolution of social insects and cheating individuals [12]. Such conflicting multilevel evolution might substantially increase the complexity of evolutionary dynamics even if different forces of evolution are constant in space and time, thereby potentially rendering the above notion of evolution inadequate [13,14,15]

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Summary

Introduction

Evolution is often conceived as changes in the properties of a population over generations [1,2,3]. License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited This consideration led us to investigate a minimal model of conflicting multilevel evolution, taking protocells as the simplest paradigm of hierarchically structured evolving systems [16 –18]. Molecules tend to evolve towards minimizing their catalytic activity k in order to maximize their relative chance of replication within a protocell—the evolution of selfish templates [7,8,20]. This tendency, if unchecked, would completely halt the replication of molecules within a protocell. A source code implementing the above model is available from Dryad (see Data accessibility)

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