Stages in the Evolution of the Cellular Information-Processing System

In Figure 1 we present a fanciful representation of the evolution of the information transfer system of modern cells and propose that it be seen as divisible into three phases, differing profoundly in both tempo and mode. The first (Figure 1 Bottom) would be accepted by all who speculate on the origin of Life as a period of preDarwinian evolution: without replication there are no entities to evolve through the agency of natural selection. We call the second period, between the appearance of the first self-replicating informational molecule and the appearance of the first "modern" cell, the period of progressive Darwinian evolution (Figure 1 Middle). "Progress" is of course an onerous concept in evolutionary theory (Ayala, 1988). Nevertheless, we submit that, as its uniquely defining feature or mode, this second phase witnessed the fixation of many mutations improving the accuracy, speed, and efficiency of information transfer overall and, thus, the adaptedness of cells (or simpler precellular units of selection) under almost any imaginable conditions. Nowadays (in the third period, that of postprogressive Darwinian evolution; Figure 1 Top), most mutations that are fixed by selection improve fitness only for specific environmental regimes. But earlier, when evolution did exhibit progress, selection forged successive generations of organisms (or simpler units) in which phenotype was more reliably coupled to genotype. Individuals from later in this period would have almost always outperformed their ancestors if placed in direct competition with them.

How could we hope to know anything about this ancient era of radically different tempo and mode? If divergences that established the major lineages of contemporary living things occurred before completion of the period of progressive Darwinian evolution, then we would expect that the information processing systems of these lineages would differ from each other—the earlier the divergence, the more profound the difference. That is, components of the replication, transcription, and translation machineries that were still experiencing progressive Darwinian evolution at the time of divergence should be differently refined or altogether separately fashioned (nonhomologous) in major lineages. Thus, comparisons between modern major groups (such as prokaryotes and eukaryotes) might lead to informed guesses about primitive ancestral states.

As an exemplary exercise, Benner and colleagues (Benner et al., 1993) inferred from the fact that archaebacteria, eubacteria, and eukaryotes produce ribonucleotide reductases that are not demonstrably homologous that their last common ancestor used a ribozyme for the reduction



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