Elsevier

Hormones and Behavior

Volume 43, Issue 1, January 2003, Pages 2-15
Hormones and Behavior

Regular article
The concept of allostasis in biology and biomedicine

https://doi.org/10.1016/S0018-506X(02)00024-7Get rights and content

Abstract

Living organisms have regular patterns and routines that involve obtaining food and carrying out life history stages such as breeding, migrating, molting, and hibernating. The acquisition, utilization, and storage of energy reserves (and other resources) are critical to lifetime reproductive success. There are also responses to predictable changes, e.g., seasonal, and unpredictable challenges, i.e., storms and natural disasters. Social organization in many populations provides advantages through cooperation in providing basic necessities and beneficial social support. But there are disadvantages owing to conflict in social hierarchies and competition for resources. Here we discuss the concept of allostasis, maintaining stability through change, as a fundamental process through which organisms actively adjust to both predictable and unpredictable events. Allostatic load refers to the cumulative cost to the body of allostasis, with allostatic overload being a state in which serious pathophysiology can occur. Using the balance between energy input and expenditure as the basis for applying the concept of allostasis, we propose two types of allostatic overload. Type 1 allostatic overload occurs when energy demand exceeds supply, resulting in activation of the emergency life history stage. This serves to direct the animal away from normal life history stages into a survival mode that decreases allostatic load and regains positive energy balance. The normal life cycle can be resumed when the perturbation passes. Type 2 allostatic overload begins when there is sufficient or even excess energy consumption accompanied by social conflict and other types of social dysfunction. The latter is the case in human society and certain situations affecting animals in captivity. In all cases, secretion of glucocorticosteroids and activity of other mediators of allostasis such as the autonomic nervous system, CNS neurotransmitters, and inflammatory cytokines wax and wane with allostatic load. If allostatic load is chronically high, then pathologies develop. Type 2 allostatic overload does not trigger an escape response, and can only be counteracted through learning and changes in the social structure.

Introduction

Modern biology provides a framework not only for understanding how the interplay of genes and environment produces individual characteristics, and how these individuals interact in social groups and with other species, but also for understanding how these interactions lead to pathophysiology and disease. For example, knowledge of how the life cycles of organisms are integrated and controlled in the natural world will allow us to assess the effects upon ecosystems of global climate change, disturbance by humans, and endocrine disrupters. Of equal importance is a need to use basic biological frameworks in human society to conceptualize and measure the cumulative impact of social status, income, education, working and living environments, lifestyle, health-related behaviors, and stressful life experiences on physical and mental health.

The daily routines of animals and humans alike include nutritional inputs to maintain normal activities and to anticipate additional requirements (e.g., breeding, migrating, acclimating to cold and heat, etc.) during the day–night cycle and the seasons. These homeostatic mechanisms, including functional and structural changes in brain and body, allow the individual to maintain physiological and behavioral stability despite fluctuating environmental conditions. Superimposed on this “predictable” life cycle are facultative physiological and behavioral responses to unpredictable events that have the potential to be stressors. These responses require extra energy procured from the environment and/or from endogenous stores of fat, glycogen, and protein. Moreover, the ability of an individual to maintain such emergency responses depends upon other factors such as parasite load, diseases, social status, permanent injury, pollution, etc. These can lead to permanent additional “costs” that potentially provide a “handicap” in the face of environmental change, unpredictable events, etc.

Historically, within both the basic biological and biomedical sciences, the concepts of stress and homeostasis have been used in ambiguous ways that obfuscate a number of important aspects of the impact of experience and genes on life cycles in general, and health and disease in particular. The energy required to fuel daily and seasonal routines includes major life history stages such as breeding, unpredictable events that can lead to stress, and the permanent handicaps accrued from disease, injury, etc. These form a continuum with important transitional points that determine whether the individual can cope or triggers facultative physiological and behavioral responses designed to reduce costs. Failure to do either results in symptoms of what we call “allostatic overload,” as discussed below.

Our goal here is to propose the inclusion of four terms, “allostasis,” “allostatic state,” “allostatic load,” and “allostatic overload” in a basic framework for the organization and management of life cycles. These terms are offered as organizing principles for understanding the management of life cycles in diverse habitats and varying degrees of unpredictability in basic biology. They also include the influence of genetic risk factors, early life events, lifestyle and health-related behaviors and stressful experiences, including social conflict and social hierarchies, on the processes of physiological adaptation and the exacerbation of disease.

The process of allostasis that leads adaptation/acclimation of the organism in the short run underlies all of what we shall discuss. We will explore how costs to the body (referred to as allostatic load) can eventually result in allostatic overload, i.e., the balance between energy expenditure and energy input. We understand fully that this is a simplistic approach and many other nutritional components (essential fatty acids and amino acids, minerals, etc.) are important. These indeed could also be modeled, but here we use the term “energy” in a very general sense that encompasses all potentially limiting resources. Moreover, we focus on glucocorticosteroids as hormonal mediators that reflect how the individual responds to the challenges imposed by the external world as well as by the internal environment. We do so in full recognition of the fact that glucocorticosteroids are only one of many interconnected hormonal mediators and that a full description of what we are outlining will require inclusion of these mediators as well.

First, we consider situations in which energy available to the organism is exceeded by demands of the environment. Second, we consider situations when energy available to the individual is not exceeded, but other factors such as social competition and conflict become paramount. Before elaborating on these ideas, we need to define some terminology.

Section snippets

Homeostasis

Homeostasis is the stability of physiological systems that maintain life, used here to apply strictly to a limited number of systems such as pH, body temperature, glucose levels, and oxygen tension that are truly essential for life and are therefore maintained within a range optimal for the current life history stage.

Allostasis

Allostasis is achieving stability through change. This is a process that supports homeostasis, i.e., those physiological parameters essential for life defined above, as

What do we mean by “stress”?

Stress is often defined as a threat, real or implied, to homeostasis. In common usage, stress usually refers to an event or succession of events that cause a response, often in the form of “distress” but also, in some cases, referring to a challenge that leads to a feeling of exhilaration, as in “good” stress. But, the term “stress” is full of ambiguities. It is often used to mean the event (stressor) or, sometimes, the response (stress response). Furthermore, it is frequently used in the

What are some examples of allostasis?

Sterling and Eyer (1988) used variations in blood pressure as an example: in the morning, blood pressure rises when we get out of bed and blood flow is maintained to the brain when we stand up in order to keep us conscious. This type of allostasis helps to maintain oxygen tension in the brain. There are other examples: catecholamine and glucocorticosteroid elevations during physical activity mobilize and replenish, respectively, energy stores needed for brain and body function under challenge.

Protection vs damage

From the standpoint of survival and health of the individual, the most important feature of mediators associated with allostasis is that they have protective effects in the short run. However, they can have damaging effects over longer time intervals if there are many adverse life events or if hormone secretion is dysregulated as in a sustained allostatic state that leads to allostatic overload (McEwen, 1998). In contrast to Selye (1956), this view holds that mediators of allostasis have a

Allostasis as a concept to unify approaches to perturbations of the environment in biological and biomedical contexts

There are potentially two complementary views of allostasis, allostatic states, allostatic load, and allostatic overload. One involves how organisms in their natural environment search for basic needs such as food and shelter, thereby enhancing overall fitness. In these cases individuals must orchestrate daily and seasonal needs in relation to environmental conditions and social status, as well as deal with unpredictable events in the environment. Failure to deal with these problems results in

Allostatic load and type 1 overload to cope with unpredictable environmental events that threaten food availability and quality of shelter—mechanisms to avoid and resist stress

All organisms must adjust their physiology, morphology, and behavior in response to changing environments — physical and social, predictable and unpredictable. This allows an individual to avoid or resist the potential for stress Sapolsky et al 2000, Wingfield et al 1998, Wingfield and Romero 2000. The rapid behavioral and physiological changes in response to perturbations have been collectively called the “emergency” life history stage, which serves to enhance lifetime fitness (Wingfield et

Allostatic load and type 2 overload—what happens when competitive social structure predominates over food and shelter as a source of challenge?

The distinction between views of Type 1 allostatic overload versus allostatic load in some forms of human disease is that increasing energy requirement is the drive leading eventually to allostatic overload when negative energy balance is reached (Ee + Ei + Eo > Eg; Fig. 1, Fig. 2). Unless the emergency life history stage reduces allostatic load (Fig. 3) to regain positive energy balance (Ee + Ei + Eo < Eg), then cumulative effects become pathological. In modern human society, we see positive

Type 2 allostatic load—a human perspective

The situations depicted in Fig. 4 are an attempt to put into an energy model the conditions that exist in the modern industrialized world with its social hierarchies and differing degrees of inequality. Modern Western society is characterized not by hunger and the search for basic creature comforts as by complex social structures. These involve living and working environments that vary in quality, variable access to recreation, and the existence of mass communications with a variety of messages

Conclusions

Most vertebrate organisms have regular patterns and routines that involve obtaining food and carrying out life history stages such as breeding, migrating, molting, hibernating, etc. These life history stages occur in set sequences on a time scale of about 1 year. Each has energetic requirements that vary according to demand. Often, life history stages such as reproduction and migration are energetically demanding, whereas others rely on stored energy only (hibernation). The annual sequence of

Acknowledgements

J.C.W. is grateful for several grants from the Division of Integrated Biology and Neuroscience, and the Office of Polar Programs, National Science Foundation. He also acknowledges a John Simon Guggenheim Fellowship, a Benjamin Meaker Fellowship (University of Bristol, UK), and a Russell F. Stark University Professorship (University of Washington). B.Mc. acknowledges the intellectual support from colleagues in the MacArthur Research Network for Socioeconomic Status and Health, Nancy Adler, UCSF,

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