The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease

https://doi.org/10.1016/j.neubiorev.2004.08.009Get rights and content

Abstract

Why do we get the stress-related diseases we do? Why do some people have flare ups of autoimmune disease, whereas others suffer from melancholic depression during a stressful period in their life? In the present review possible explanations will be given by using different levels of analysis.

First, we explain in evolutionary terms why different organisms adopt different behavioral strategies to cope with stress. It has become clear that natural selection maintains a balance of different traits preserving genes for high aggression (Hawks) and low aggression (Doves) within a population. The existence of these personality types (Hawks–Doves) is widespread in the animal kingdom, not only between males and females but also within the same gender across species.

Second, proximate (causal) explanations are given for the different stress responses and how they work. Hawks and Doves differ in underlying physiology and these differences are associated with their respective behavioral strategies; for example, bold Hawks preferentially adopt the fight–flight response when establishing a new territory or defending an existing territory, while cautious Doves show the freeze–hide response to adapt to threats in their environment. Thus, adaptive processes that actively maintain stability through change (allostasis) depend on the personality type and the associated stress responses.

Third, we describe how the expression of the various stress responses can result in specific benefits to the organism.

Fourth, we discuss how the benefits of allostasis and the costs of adaptation (allostatic load) lead to different trade-offs in health and disease, thereby reinforcing a Darwinian concept of stress. Collectively, this provides some explanation of why individuals may differ in their vulnerability to different stress-related diseases and how this relates to the range of personality types, especially aggressive Hawks and non-aggressive Doves in a population.

A conceptual framework is presented showing that Hawks, due to inefficient management of mediators of allostasis, are more likely to be violent, to develop impulse control disorders, hypertension, cardiac arrhythmias, sudden death, atypical depression, chronic fatigue states and inflammation. In contrast, Doves, due to the greater release of mediators of allostasis (surplus), are more susceptible to anxiety disorders, metabolic syndromes, melancholic depression, psychotic states and infection.

Section snippets

General introduction

Due to the pioneering work of Hans Selye [1], the use of the word ‘Stress’ has become popular all over the world. However, despite the vast amount of scientific research generated in this field the term stress has been a stumbling block right from its first use. The term has so many different meanings [2] that it becomes counterproductive by inhibiting a proper application and critical interpretation of experimental results. Stress has mostly been associated with negative events and

Theoretical considerations: evolutionary stable strategies

Why do organisms adopt different behavioral strategies for coping with stress? The question arises why variation is maintained in a population or why a population does not simply drift towards a homogeneous group of the most successful phenotypes. There is some theoretical support for the maintenance of individual variation within a population. For instance, Maynard Smith [16] applied ‘Game Theory’ to animal behavior and found that natural selection tends to maintain a balance between different

Neuroendocrine differences between Hawks and Doves

In order to adapt to a changing environment Hawks and Doves not only differ in the type of behavioral responses shown, i.e. fight–flight versus freeze–hide, but also in their underlying physiology, neuroendocrinology (Table 2) and neurobiology (Table 3). We provide proximate (causal) explanations for the requirement for different stress responses and for how they exert their actions. First though, we list the differences in the physiological responses of Hawks and Doves (3.1 Neuroendocrine

Allostatic state, allostatic load and the emotional brain

Mediators of allostasis (e.g. adrenal hormones, neurotransmitters, and immuno-cytokines) act on receptors in various tissues and organs to produce effects that are adaptive in the short term but that can produce an allostatic state which may be damaging if the mediators are not shut off. Allostatic state refers to a state of chronic deviation of the regulatory system from its normal mean operating level [9]. As a result, the effects of the different mediators on target cells are prolonged and

Conclusions

With the exception of the past few thousand years, a drop in the bucket of evolutionary time, humans and animals have evolved in natural habitats and are therefore intricately tied to nature. It has become clear that natural selection maintains a balance of different traits, e.g. preserving genes for high aggression (Hawks) and low aggression (Doves) within a population. The existence of the Hawk–Dove strategy is widespread in the animal kingdom, not only between males and females, but also

Acknowledgements

We thank Dr Bryan Jones for helpful criticism of the manuscript.

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