Abstract
Many biological processes can be thought of as the result of an underlying
dynamics in which the system repeatedly undergoes distinct and abortive
trajectories with the dynamical process only ending when some specific process,
purpose, structure or function is achieved. A classic example is the way in
which microtubules attach to kinetochores as a prerequisite for chromosome
segregation and cell division. In this example, the dynamics is characterized
by apparently futile time histories in which microtubules repeatedly grow and
shrink without chromosomal attachment. We hypothesize that for biological
processes for which it is not the initial conditions that matter, but rather
the final state, this kind of exploratory dynamics is biology's unique and
necessary solution to achieving these functions with high fidelity. This kind
of cause and effect relationship can be contrasted to examples from physics and
chemistry where the initial conditions determine the outcome. In this paper, we
examine the similarities of many biological processes that depend upon random
trajectories starting from the initial state and the selection of subsets of
these trajectories to achieve some desired functional final state. We begin by
reviewing the long history of the principles of dynamics, first in the context
of physics, and then in the context of the study of life. These ideas are then
stacked against the broad categories of biological phenomenology that exhibit
exploratory dynamics. We then build on earlier work by making a quantitative
examination of a succession of increasingly sophisticated models for
exploratory dynamics, all of which share the common feature of being a series
of repeated trials that ultimately end in a "winning" trajectory. We also
explore the ways in which microscopic parameters can be tuned to alter
exploratory dynamics as well as the energetic burden of performing such
processes.