Co-option of stress mechanisms in the origin of evolutionary novelties

It is widely accepted that stressful conditions can facilitate evolutionary change. The mechanisms elucidated thus far accomplish this with a generic increase in heritable variation that facilitates more rapid adaptive evolution, often via plastic modifications of existing characters. Through scrutiny of different meanings of stress in biological research, and an explicit recognition that stressors must be characterized relative to their effect on capacities for maintaining functional integrity, we distinguish between: (1) previously identified stress-responsive mechanisms that facilitate evolution by maintaining an adaptive fit with the environment, and (2) the co-option of stress-responsive mechanisms that are specific to stressors leading to the origin of novelties via compensation. Unlike standard accounts of gene co-option that identify component sources of evolutionary change, our model documents the cost-benefit trade-offs and thereby explains how one mechanism-an immediate response to acute stress-is transformed evolutionarily into another-routine protection from recurring stressors. We illustrate our argument with examples from cell type origination as well as processes and structures at higher levels of organization. These examples suggest a general principle of evolutionary origination based on the capacity to switch between regulatory states related to reproduction and proliferation versus survival and differentiation.

Automated summary

It is widely accepted that stressful conditions can facilitate evolutionary change by increasing heritable variation and promoting rapid adaptive evolution. Stressors can be categorized into two types based on their effect on functional integrity: stress-responsive mechanisms that maintain adaptive fit with the environment, and stress-responsive mechanisms specific to stressors that lead to the emergence of novelties through compensation. Our model explains the evolutionary transformation of an immediate response to acute stress into routine protection from recurring stressors by considering cost-benefit trade-offs. Examples from different levels of organization support the general principle of evolutionary origination based on the ability to switch between regulatory states related to reproduction and survival.