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Background  The origins of life on the Earth required chemical entities to interact with their environments in ways that could respond to natural selection. The concept of interpretation, where biotic entities use signs in their environment as proxy for the existence of other items of selective value in their environment, has been proposed on theoretical grounds to be relevant to the origins and early evolution of life. However this concept has not been demonstrated empirically.    Results  Here, we present data that certain catalytic RNA sequences have properties that would enable interpretation of divalent cation levels in their environment. By assaying the responsiveness of two variants of the  Tetrahymena  ribozyme to the Ca 2+  ion as a sign for the more catalytically useful Mg 2+  ion, we show an empirical proof-of-principle that interpretation can be an evolvable trait in RNA, often suggested as a model system for early life. In particular we demonstrate that  in vitro , the wild-type version of the  Tetrahymena  ribozyme is not interpretive, in that it cannot use Ca 2+  as a sign for Mg 2+ . Yet a variant of this sequence containing five mutations that alter its ability to utilize the Ca 2+  ion engenders a strong interpretive characteristic in this RNA.    Conclusions  We have shown that RNA molecules in a test tube can meet the minimum criteria for the evolution of interpretive behaviour in regards to their responses to divalent metal ion concentrations in their environment. Interpretation in RNA molecules provides a property entirely dependent on natural physico-chemical interactions, but capable of shaping the evolutionary trajectory of macromolecules, especially in the earliest stages of life’s history.

Empirical demonstration of environmental sensing in catalytic RNA: evolution of interpretive behavior at the origins of life