What is in a name? Integrating homeostasis, allostasis and stress.

All organisms must adjust morphology, physiology and behavior as they go about their life cycles. For vertebrates, including humans, these adjustments occur as daily routines and in many cases, as seasonal routines as well. Superimposed on this predictable life cycle are unpredictable events, including many potential stressors, requiring immediate physiological and behavioral adjustments to cope. Additionally, infection, disease, age, old injuries, social status etc. may influence how an individual goes about its life cycle routines and responds to unpredictable perturbations. The classic concept of homeostasis (sensu Cannon, 1932) is fundamental to these adjustments. However, unless we have misinterpreted or overlooked something, homeostasis in its pure form does not incorporate adequately all of the processes involved and we believe that it is very useful to have supplemental terminology such as the allostasis concept in view of the many ambiguities of the uses of the words “homeostasis” as well as “stress”. For example, a cow that begins lactation undergoes morphological, physiological and behavioral changes so it can raise a calf. None of this is essential for the maintenance of homeostasis of the cow, although homeostatic set points will have changed from pre-lactation levels (Baumann, 2000). Another example is the migration of a songbird from Mexico to Alaska in spring and back again in autumn. Here again there are major changes in morphology, physiology and behavior that allow this animal to complete a journey of almost 5000 Km in less than a month. But none of this is essential for maintenance of homeostasis. In both examples, the process of preparing for lactation or migration involves regulation of gene expression. Furthermore, termination of lactation and migration involves turning off of many genes involved. Of course both the cow lactating and the songbird migrating must do so to reproduce successfully. But the adjustments in homeostasis that occur during these life cycle events are to accommodate changed physiology as part of the predictable life cycle, not simply responses to deviations from some set point that maintains life processes. It is also important to bear in mind that changes in morphology, physiology and behavior associated with life cycle events such as lactation and migration also alter the responsiveness of the individual to unpredictable, and potentially stressful, events. Usually, a process such as lactation or migration results in the individual becoming more susceptible to perturbations of the environment, and adjustments in the stress response are made in anticipation of this. As far as we know, the classic concept of homeostasis does not incorporate all of these processes – homeostasis of daily routines, responses to perturbations, changed susceptibility to those perturbations and anticipatory adjustments to cope with them for at least part of the life cycle. Furthermore, there is growing evidence that many organisms change their sensitivity to stresses temporarily (e.g. when breeding, Wingfield and Sapolsky, 2003) by adjusting secretions of mediators of allostasis that help maintain homeostasis (such as glucocorticoids). At first this seems counter intuitive, but temporary suspension of the classic stress response (and homeostatic adjustments in response to a perturbation) allows an individual to breed successfully, but the trade-off is potential permanent damage owing to the failure to show immediate responses that would normally promote adaptation. How do we model this apparently frequent strategy? It is in this context that we offer some ideas and responses to the article by Romero and colleagues (2009) who present a different terminology and a new model for conceptualizing and describing the impact of stress on the body, combining traditional notions of stress and homeostasis with the more recent terminology of allostasis and allostatic load. It is our specific goal to point out where the concept of allostasis adds to the concept of homeostasis but also presents a framework by which to incorporate major events of the predictable life cycle (such as reproduction, migration etc.) with perturbations and the potential for stress. In our opinion, certain aspects of this formulation, summarized below, will be a useful addition to the ongoing discussion of this topic, but first some conceptual issues must be addressed that also involve semantics.