'The Arrival of the Fittest': Toward a Theory of Biological Organization

Walter Fontana and Leo W. Buss

The formal structure of evolutionary theory is based upon the dynamics of alleles, individuals and populations. As such, the theory must assume the prior existence of these entities. This existence problem was recognized nearly a century ago, when DeVries (1904) stated, "Natural selection may explain the survival of the fittest, but it cannot explain the arrival of the fittest." At the heart of the existence problem is determining how biological organizations arise in ontogeny and in phylogeny.

We develop a minimal theory of biological organization based on two abstractions from chemistry. The theory is formulated using -calculus, which provides a natural framework capturing (i) the constructive feature of chemistry, that the collision of molecules generates new molecules, and (ii) chemistry's diversity of equivalence classes, that many different reactants can yield the same stable product. We employ a well-stirred and constrained stochastic flow reactor to explore the generic behavior of large numbers of applicatively interacting -expressions. This constructive dynamical system generates fixed systems of transformation characterized by syntactical and functional invariances.

Organizations are recognized and defined by these syntactical and functional regularities. Objects retained within an organization are characterized by a grammar and interactions among objects by algebraic relationships. The objects which maintain themselves in the system realize an algebraic structure and possess a grammar which is invariant under the interaction between objects. An organization is self-maintaining, and is characterized by (i) boundaries established by the invariances, (ii) strong self-repair capabilities responsible for a robustness to perturbation, and (iii) a center, defined as the smallest set kinetically persistent and self-maintaining generator set of the algebra.

Imposition of different boundary conditions on the stochastic flow reactor generates different levels of organization, and a diversity of organizations within each level. Level 0 is defined by self-copying objects or simple ensembles of copying objects. Level 1 denotes a new object class, whose objects are self-maintaining organizations made of Level 0 objects, and Level 2 is defined by self-maintaining metaorganizations composed of Level 1 organizations.

These results invite analogy to the history of life, that is, to the progression from self-replication to self-maintaining procaryotic organizations to ultimately yield self-maintaining eucaryotic organizations. In our system self-maintaining organizations arise as a generic consequence of two features of chemistry, without appeal to natural selection. We hold these findings as calling for increased attention to the structural basis of biological order.