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Transfer RNA (tRNA) molecules play vital roles during protein synthesis. Their acceptor arms are aminoacylated with specific amino acid residues while their anticodons delimit codon specificity. The history of these two functions has been generally linked in evolutionary studies of the genetic code. However, these functions could have been differentially recruited as evolutionary signatures were left embedded in tRNA molecules. Here we built phylogenies derived from the sequence and structure of tRNA, we forced taxa into monophyletic groups using constraint analyses, tested competing evolutionary hypotheses, and generated timelines of amino acid charging and codon discovery. Charging of Sec, Tyr, Ser and Leu appeared ancient, while specificities related to Asn, Met, and Arg were derived. The timelines also uncovered an early role of the second and then first codon bases, identified codons for Ala and Pro as the most ancient, and revealed important evolutionary take-overs related to the loss of the long variable arm in tRNA. The lack of correlation between ancestries of amino acid charging and encoding indicated that the separate discoveries of these functions reflected independent histories of recruitment. These histories were probably curbed by co-options and important take-overs during early diversification of the living world.

Evolutionary Patterns in the Sequence and Structure of Transfer RNA: A Window into Early Translation and the Genetic Code