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Mechanisms of Evolutionary Innovation Point to Genetic Control Logic as the Key Difference Between Prokaryotes and Eukaryotes

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Abstract

The evolution of life from the simplest, original form to complex, intelligent animal life occurred through a number of key innovations. Here we present a new tool to analyze these key innovations by proposing that the process of evolutionary innovation may follow one of three underlying processes, namely a Random Walk, a Critical Path, or a Many Paths process, and in some instances may also constitute a “Pull-up the Ladder” event. Our analysis is based on the occurrence of function in modern biology, rather than specific structure or mechanism. A function in modern biology may be classified in this way either on the basis of its evolution or the basis of its modern mechanism. Characterizing key innovations in this way helps identify the likelihood that an innovation could arise. In this paper, we describe the classification, and methods to classify functional features of modern organisms into these three classes based on the analysis of how a function is implemented in modern biology. We present the application of our categorization to the evolution of eukaryotic gene control. We use this approach to support the argument that there are few, and possibly no basic chemical differences between the functional constituents of the machinery of gene control between eukaryotes, bacteria and archaea. This suggests that the difference between eukaryotes and prokaryotes that allows the former to develop the complex genetic architecture seen in animals and plants is something other than their chemistry. We tentatively identify the difference as a difference in control logic, that prokaryotic genes are by default ‘on’ and eukaryotic genes are by default ‘off.’ The Many Paths evolutionary process suggests that, from a ‘default off’ starting point, the evolution of the genetic complexity of higher eukaryotes is a high probability event.

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Notes

  1. WB personal observation from BLAST searches using NP_011365.1 (yeast INO80), EDN63720.1 (yeast SW1/SNF) BAG10015.1 (human INO80) and BAG10565.1 (human SW1/SNF) on NCBI protein database excluding Eukarya from the target database.

  2. We realize that this is a rather simplified view of the constraints on the evolution of gene control mechanisms. One could, for example, imagine the evolution of a mechanism in a prokaryote from an RNA that interacted with no genes to one that interacted with only one, thence with two and so on. However, a myriad of in vitro protein and RNA evolution experiments show us that it is easier to find a macromolecule that interacts weakly with many things, and then refine its specificity by selection, than it is to find a macromolecule that interacts specifically (and hence tightly) with just one molecule in one step.

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Acknowledgments

We are grateful to Janusz Petkowski (ETH Zurich, Switzerland) for helpful comments on an earlier formulation of this paper, David Simpson (Glythera Ltd, UK) for help with expression systems, to several anonymous readers and reviewers for their comments, and Mike Danson (University of Bath, UK) for pointers to the literature on archaeal expression systems.

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Correspondence to William Bains.

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The authors received no funding for this work and have no conflict of interest to declare.

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Bains, W., Schulze-Makuch, D. Mechanisms of Evolutionary Innovation Point to Genetic Control Logic as the Key Difference Between Prokaryotes and Eukaryotes. J Mol Evol 81, 34–53 (2015). https://doi.org/10.1007/s00239-015-9688-6

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  • DOI: https://doi.org/10.1007/s00239-015-9688-6

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