Molecular complementarity I: the complementarity theory of the origin and evolution of life.

We assert that molecular complementarity is much more widespread than is commonly acknowledged in biological systems, if not actually ubiquitous. It creates the coupling necessary for non-equilibrium systems to form. It stabilizes aggregates against degradation, thereby increasing concentrations to levels adequate to foster the formation of prebiotic systems and represents the earliest form in which natural selection was manifested. Complementarity confers on all interacting parts of such systems in formation carrying capacity. RNA or DNA are not, therefore, necessary to the emergence of life, but represent specialized forms of complementary molecules adapted specifically to information storage and transmission. Non-genetic information exists in metabolic functions and probably preceded genetic information historically. Complementarity also provides the basis for homeostasis and buffering of such systems not only in a chemical, but also in structural and temporal terms. It provides a mechanism for understanding how new, emergent properties can arise, and a basis for the self-organization of systems. We demonstrate that such aggregates can have properties not predictable from their individual components, thus providing a means for understanding how new functions emerge during evolution. Selection is for modules rather than individual components. The formation of functional sub-systems that can then be integrated as modules greatly increases the probability of the emergence of life. The result of such modular evolution alters the standard view of evolution from a tree or bush-like image to an integrated network composed of alternating periods of integration (as molecules and molecular aggregates merge) and divergence (as molecules and aggregates undergo variations). This provides a mechanism for evolution by punctuated equilibria. Molecular complementarity puts strict limits on variations, however, preventing evolution from being random. The evolutionary, physiological and embryological consequences of this view of life are outlined, and various models and experiments described that further characterize it. Copyright 1997 Academic Press Limited Copyright 1997.