How and why kinetics, thermodynamics, and chemistry induce the logic of biological evolution

Abstract

Thermodynamic stability, as expressed by the Second Law, generally constitutes the driving force for chemical assembly processes. Yet, somehow, within the living world most self-organisation processes appear to challenge this fundamental rule. Even though the Second Law remains an inescapable constraint, under energy-fuelled, far-from-equilibrium conditions, populations of chemical systems capable of exponential growth can manifest another kind of stability, dynamic kinetic stability (DKS). It is this stability kind based on time/persistence, rather than on free energy, that offers a basis for understanding the evolutionary process. Furthermore, a threshold distance from equilibrium, leading to irreversibility in the reproduction cycle, is needed to switch the directive for evolution from thermodynamic to DKS. The present report develops these lines of thought and argues against the validity of a thermodynamic approach in which the maximisation of the rate of energy dissipation/entropy production is considered to direct the evolutionary process. More generally, our analysis reaffirms the predominant role of kinetics in the self-organisation of life, which, in turn, allows an assessment of semi-quantitative constraints on systems and environments from which life could evolve.

Keywords: dynamic kinetic stability; kinetic control; origins of life; self-organisation.

Figure 1

Self-assembly. (A) Macromolecular structures or patterns can form as the result of binding energy being released through the interaction of units which compensates for the decrease in entropy associated with self-organisation. (B) An example of dissipative self-assembly of reactants unable to react in the ground state but which can be activated to yield unstable reactive units (e.g., susceptible to hydrolysis). The supramolecular structure is dynamically stable as long as the system is held far from equilibrium through the energy-fuelled supply of reactive units.

Figure 2

Kinetic control. In many chemical reactions leading to different products, the final composition is determined by the height of the kinetic barriers corresponding to transition states (TS^‡₁ and TS^‡₂) rather than by the relative free energies of reactant (R) and products (P₁ and P₂). Under kinetic control, P₂ would be favoured over P₁.

Figure 3

Evolution of an autocatalytic network involving a parasite. R: resource; A: autocatalyst; B: predator autocatalyst.

Figure 4

Numerical simulation of the system of Figure 3 (k₀ = 0.01 M min⁻¹, k₁ = 0.02 min⁻¹, k₂ = 0.4 M⁻¹ min⁻¹, k₃ = 0.04 min⁻¹, k₄ = 1.2 M⁻¹ min⁻¹ and k₅ = 0.04 min⁻¹). (A) Evolution of the concentrations of resource (R), autocatalyst (A) and predator (B) species; (B) flux of product formation through the autocatalytic system from A and B. The initial concentrations [R] = [A] = [B] = 0 were selected. After [R] approaches a steady state ([R]_*1 = k₀/k₁ = 0.5 M), at 300 min 10⁻⁶ M A is added leading to a new steady state ([R]_*2 = k₃/k₂ = 0.1 M and [A]_*2 = (k₀ − k₁ × k₃/k₂)/k₃ = 0.2 M). A new regime is initiated by the addition of 10⁻⁶ M B at 600 min (steady state [A]_*3 = k₅/k₄ = 0.033 M and [R]_*3 = k₀/(k₁ + k₂ k₅/k₄) = 0.3 M). Simulation results were not changed using a twice-shorter interval of time between iterations (0.5 min instead of 1 min).

Figure 5

The Raleigh–Bénard instability. Convection takes place in a liquid layer provided that the temperature difference between the bottom and the top of the layer exceeds a threshold value.