Selectively advantageous instability in biotic and pre-biotic systems and implications for evolution and aging.

Abstract

Rules of biology typically involve conservation of resources. For example, common patterns such as hexagons and logarithmic spirals require minimal materials, and scaling laws involve conservation of energy. Here a relationship with the opposite theme is discussed, which is the selectively advantageous instability (SAI) of one or more components of a replicating system, such as the cell. By increasing the complexity of the system, SAI can have benefits in addition to the generation of energy or the mobilization of building blocks. SAI involves a potential cost to the replicating system for the materials and/or energy required to create the unstable component, and in some cases, the energy required for its active degradation. SAI is well-studied in cells. Short-lived transcription and signaling factors enable a rapid response to a changing environment, and turnover is critical for replacement of damaged macromolecules. The minimal gene set for a viable cell includes proteases and a nuclease, suggesting SAI is essential for life. SAI promotes genetic diversity in several ways. Toxin/antitoxin systems promote maintenance of genes, and SAI of mitochondria facilitates uniparental transmission. By creating two distinct states, subject to different selective pressures, SAI can maintain genetic diversity. SAI of components of synthetic replicators favors replicator cycling, promoting emergence of replicators with increased complexity. Both classical and recent computer modeling of replicators reveals SAI. SAI may be involved at additional levels of biological organization. In summary, SAI promotes replicator genetic diversity and reproductive fitness, and may promote aging through loss of resources and maintenance of deleterious alleles.