On the Thermodynamics of Evolution

ON THE THERMODYNAMICS OF EVOLUTION SIMON BLACK* In a popular article entitled "Darwin's Mistake" [1], Bethell contends that the concept of natural selection rests precariously on circular reasoning : Species survive because they are fit, and they are fit because they survive. Implied in his argument is a legitimate demand that Darwin's defenders show a more fundamental criterion for survival. This demand goes to the heartofthe evolutionary mystery because it is another way of asking why life exists. I shall develop the idea that life arose from inanimate matter for thermodynamic reasons, and that the fundamental criterion for survival is the capacity of organisms to accelerate the dissipation of free energies in organic chemical-water systems. The hypothesis provides: (i) a physicochemical definition of evolutionary fitness, (ii) a spontaneous beginning for the evolutionary process, and (iii) a thermodynamic and stereochemical basis for the origin of the genetic code. It also accounts for (iv) the immense catalytic power of enzymes, (v) the survival of species despite death of individual organisms , and (vi) the coupling process through which degradative energy from certain substances supports the synthesis of others. General Considerations In the evolutionary process, matter changes at the chemical level, the molecular makeup of each generation being slightly different from that of the preceding one. If it is assumed that this process is in any fundamental way different from inanimate processes, it follows inexorably that life could not have spontaneously arisen from nonliving matter. The creationist assumption of divine origin is the only known alternative. On the other hand, if it is assumed that evolution involves no principles other than those of physics and chemistry, the origin and evolution of organisms must be explicable in physicochemical terms. ?Laboratory of Biochemical Pharmacology, National Institute of Arthritis, Metabolism, and Digestive Diseases, National Institutes of Health, Bethesda, Maryland 20014. I am grateful to Drs. Anthony V. Furano and Kehl Markley for critical reviews of the manuscript .© 1978 by The University of Chicago. 0031-5982/78/2103-0026$01.00 348 I Simon Black ¦ Thermodynamics ofEvolution All physicochemical processes involve a degradation or dissipation of free energy, and the free energy available for a process is often called its driving force. If the evolutionary conversion of inanimate matter to progressively more complex living structures is indeed a physicochemical process, then it too must have a driving force. Each evolutionary step, which appears to us superficially as a "selection for fitness," must result from a thermodynamic pressure and be accompanied by an expenditure of free energy. This is an inescapable deduction. In any natural process the dissipation of free energy is accompanied by a net increase in entropy, which is mathematically equivalent to a decrease in information. For example, in the conversion of water to ice the liberated heat causes a rise in the entropy of the remainder of the universe, and this rise exceeds in value the decrease in entropy due to the formation of the ordered structure of ice from the less ordered water. The information of the water increases on freezing, but the information of the remaining universe decreases to a more than compensating degree. Similarly, the increase in information accompanying the formation of living cellular substance from nutrients is more than compensated by the metabolic degradation of information in other nutrients . All biochemical knowledge attests that living systems are in no way different from inanimate ones in any physicochemical sense. Despite the physicochemical correspondence of living and nonliving systems, many recent speculations tacitly or even frankly assume that in organisms information is somehow more important than free energy, and that the capacity to accumulate and preserve information is a unique attribute of the life process. There has been no reconciliation of these ideas with the second law of thermodynamics. In this article it is assumed that the origin of life can be understood in terms of established principles of physics and chemistry. It is concluded that evolution is driven by the free energies that arise when organic compounds interact with water, and that information accumulates in DNA by selection for high energydissipating velocity in the integrated life process that DNA encodes. Natural selection from large pools of widely variant alleles that accumulate...