The evolution of barriers to exploitation: Sometimes the Red Queen can take a break.

Abstract

We propose a general barrier theory as an evolutionary framework for understanding coevolutionary effects of conflicts of interest in natural and human systems. It is generalized from the barrier theory of cancer, which describes how cancer develops through the evasion of mechanisms, that block unregulated cellular reproduction and survival. Barriers are naturally evolved or artificially implemented mechanisms for blocking exploitation; restraints are mechanisms that impede but do not block exploitation. When conflicts of interest arise, selection will favor exploiters that are capable of overcoming barriers and restraints. When barriers are in place, they halt, at least temporarily, coevolutionary arms races (the Red Queen can stop running). Barriers occur in a broad spectrum of interactions characterized by conflicts of interest: barriers to cellular survival (apoptosis) and reproduction (cell cycle arrest) may block a virus from replicating its genome through reproduction of its host cell. Vaccines may completely protect against targeted pathogens. A plant may escape herbivory by evolving defensive chemicals that block herbivory. Obligate mutualisms may evolve when barriers to horizontal transmission favor symbionts that increasingly lose mechanisms that contribute to horizontal transmission. Here, we show how the barrier theory applies across a spectrum of natural and social systems.