Evolutionary layering and the limits to cellular perfection

Abstract

Although observations from biochemistry and cell biology seemingly illustrate hundreds of examples of exquisite molecular adaptations, the fact that experimental manipulation can often result in improvements in cellular infrastructure raises the question as to what ultimately limits the level of molecular perfection achievable by natural selection. Here, it is argued that random genetic drift can impose a strong barrier to the advancement of molecular refinements by adaptive processes. Moreover, although substantial improvements in fitness may sometimes be accomplished via the emergence of novel cellular features that improve on previously established mechanisms, such advances are expected to often be transient, with overall fitness eventually returning to the level before incorporation of the genetic novelty. As a consequence of such changes, increased molecular/cellular complexity can arise by Darwinian processes, while yielding no long-term increase in adaptation and imposing increased energetic and mutational costs.genetic load | cellular evolution | robustness | nonadaptive evolution A lthough natural selection is one of the most powerful forces in the biological world, it is not all powerful. However, so ingrained is the belief in the extraordinary power of selection that when confronted by biological imperfections at the molecular and morphological levels, most investigators simply invoke pleiotropic constraints, i.e., negative functional relationships between two traits influenced by the same genes, resulting from molecular limitations, metabolic tradeoffs, etc. When made in the absence of any direct evidence, as is often the case, such adherence to the adaptationist paradigm discourages the likelihood of recognizing nonadaptive paths to the origin of organismal features (1-3).Random genetic drift imposes a fundamental constraint on the level of perfection achievable by natural selection. As a consequence of the finite sampling of gametes and the linked nature of genomes, all populations experience stochastic fluctuations in allele frequencies that compromise the efficiency of selection. Once a high enough level of molecular perfection has been achieved so that further refinements in fitness are smaller than the prevailing force of drift, natural selection will be incapable of promoting any additional improvement (4, 5). Depending on the nature of the potential genetic variation underlying an adaptation, this drift barrier may be reached before selection is confronted with any physical, chemical, or bioenergetic constraints.If, however, drift prevents natural selection from inexorably moving cellular features toward a state of molecular perfection, how do we account for the abundant examples of organisms using layered mechanisms for dealing with intracellular problems? For example, genome replication involves highly selective DNA polymerases, but the small fraction of initial base misincorporations are subject to correction by subsequent proofreading, and the still smaller fraction of errors that escape ...

Evolutionary diversification of the multimeric states of proteins

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Analog nitrogen sensing inEscherichia colienables high fidelity information processing

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Evolutionary cell biology: Two origins, one objective

“…Most notable among these factors is random genetic drift, which imposes noise in the evolutionary process owing to the finite numbers of individuals and chromosome architecture. Such stochasticity leads to the drift-barrier hypothesis for the evolvable limits to molecular refinement (28,29), which postulates that the degree to which natural selection can refine any adaptation is defined by the genetic effective population size. One of the most dramatic examples of this principle is the inverse relationship between levels of replication fidelity and the effective population sizes of species across the Tree of Life (30).…”