Function as a constraint on mechanism

Box 3.5 Behavioural rhythmicity

3.5 Mechanism and constraint

3.5.2 Function as a constraint on mechanism

An animal’s resources are in demand for several competing activities. No activity, there-fore, can command total investment. Instead, it is assumed that tradeoffs occur between conflicting priorities so that the animal maximises its lifetime reproductive success within the constraint of its limited resources (see 2.4.5). This applies as much to the anatomical and physiological machinery of behaviour as to any other characteristic (Ricklefs & Wikelski 2002). In addition, a particular mechanism, such as a neural net-work or hormone, may be involved in the control of a number of different activities whose demands also conflict. There are thus different ways in which functional demands may constrain mechanism. We shall illustrate the point by considering potential conflicts between functions regulated by testosterone.

3.5.2.1 Testosterone, immunity and behaviour

As we have seen, testosterone and other sex steroids are important mediators of a wide range of behaviours. Apart from their effects on behaviour and reproductive physiology, however, sex steroids also affect the immune system in ways that may conflict with, and thus cause downregulation of, their other activities. Hormone-mediated interactions between the immune system and the CNS have been known for a long time, and provide mechanisms by which psychological state and behaviour can influence immunocom-petence and vice versa – the field of psychoneuroimmunology (Maier & Watkins 1999;

Ader et al. 2001). More recently, however, interest has centred on the signiﬁcance of this bidirectional relationship from a functional and evolutionary perspective (Folstad

& Karter 1992; Sheldon & Verhulst 1996; Barnard & Behnke 2001). Evolutionary biol-ogists interested in the role of parasites and disease in sexual selection have focused on the immunomodulatory effects of steroid hormones, particularly testosterone, involved in the development of some secondary sexual characters and behaviours (10.1.3.2).

While this has spawned a research industry of its own, it has also fuelled a more general interest in hormone-mediated tradeoffs between immunity and behaviour (Sheldon &

Verhulst 1996; Beckage 1997; Barnard & Behnke 2001). Barnard and Behnke (2001) have studied such tradeoffs in relation to social status in laboratory mice.

Barnard and Behnke argue that dominant and subordinate male mice represent differ-ent life history strategies cdiffer-entring on competitive ability. Competitive dominant males can command access to limited resources such as food and nesting sites and invest heavily in the reproductive opportunities this brings. Less competitive subordinate males cannot compete for resources so have to make do with sneaking opportunistic matings as and when they can (see ‘best of a bad job’ strategies in 2.4.5.1). A prediction that follows from this is that dominant males will be more likely to trade off future survival for short-term reproductive opportunity than subordinates, who would do better to safeguard survival and maximise the likelihood of chance matings. One way of regulating the tradeoff between reproduction and future survival might be to link the secretion of immuno-depressive sex steroids to current immunocompetence – i.e. secrete testosterone only if your immune system is robust. Barnard et al. (1996a) found that subordinate males did exactly this by regulating the secretion of testosterone in relation to their current circulating anti-body levels (one measure of immunocompetence) (Fig. 3.37a). As a result, their resistance to a subsequent infection was unaffected by testosterone (Fig. 3.37b). Dominants, on the other hand, did not regulate their secretion of testosterone in relating to antibody levels, with the result that testosterone reduced their subsequent resistance to infection (Fig. 3.37c,d).

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Further support for the adaptive immunity tradeoff idea came from experimentally immunodepressed males. In these, both testosterone levels and behaviours such as aggres-sion and locomotory activity, which tend to depress immunity, were downregulated, while sleep, which tends to enhance immunity, went up, regardless of social status (Barnard et al. 1997a). The really telling point, however, was that the regulation of both Figure 3.37 Secretion of testosterone in male laboratory mice depends on both social status and current immuno-competence. Subordinate males tend to secrete testosterone only when their current antibody titre is high (a), thus avoiding a testosterone-dependent reduction in resistance (% red blood cells infected) to an experimental infection of the blood protozoan parasite Babesia microti (b). Dominant males, in contrast, secrete testosterone regardless of current immunocompetence (c) and do suffer a testosterone-dependent reduction in resistance (d). Vertical axis scales are deviations from sample means. Modiﬁed from Barnard et al. (1996a).

testosterone and behaviours affecting immunity in depressed males was abolished when female odours (suggesting reproductive opportunity) were present in the environment (Barnard et al. 1997b).

Taken together, therefore, these results suggest that males bring costly physiological mechanisms into action only if it is reproductively worthwhile to do so. Thus dominants are more prepared to risk their future survival by secreting testosterone than subordinates because they are in a better position to secure matings in the short term. However, both classes of male are prepared to risk it if current reproductive opportunity seems high enough (there is lots of female odour about). In this case, therefore, functional considera-tions appear to limit the deployment of a physiological mechanism.

Summary

1. In most animals, behaviour patterns reflect the complexity and functional organisation of the nervous system. As we ascend the evolutionary scale, nervous systems show two major trends: towards greater differentiation and greater centralisation. Comparative studies show that many adaptive differences in behaviour are reflected in the gross anatomy of the central nervous system, some aspects of which are influenced by the behavioural history of the individual.

2. Some adaptive behaviour patterns can be traced to speciﬁc neural pathways, with eventual motor responses sometimes under the control of a hierarchy of ‘command centres’. In many cases, however, the control of behaviour is not a local, self-contained process, but the result of a distributed neural network functioning in different ways at different times. Computer and robotic simulations are providing revealing new ways of modelling the neural control of behaviour.

3. Neural control mechanisms coordinate the animal’s response to events in its environ-ment. However, the nervous system is not a passive observer of such events. Stimuli from the environment are filtered through the animal’s sense organs and processed by its nervous system so that the animal obtains a biased view of the world shaped by natural selection. We can thus think of animals having perceptual rules of thumb which reflect the reproductive costs and benefits of perceiving the world in different ways.

4. Hormones transmit information around the body more slowly than nerve cells. Together, the rapid responses of the nervous system and more sustained influences of hormones complement one another in controlling the animal’s actions. Hormones influence beha-viour through a variety of routes, including the nervous system, sensory perception, effector systems and development. However, their effects are themselves influenced by a wide range of factors, from individual genotype and experience to seasonal, ecological and life history factors.

5. The interaction between neural and hormonal inﬂuences is shown particularly clearly in the entrainment and control of rhythmic behaviour patterns associated with environ-mental cycles. Together they provide animals with an adaptive internal clock which is regulated to relevant external cyclical events.

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6. Function and mechanism can mutually constrain one another. Examples of constraints on function can be seen in perceptual biases and mechanical constraints, while hormone-mediated immunity tradeoffs show how functional considerations can limit the deployment of hormonal control mechanisms.

Box 3.5 Behavioural rhythmicity

3.5 Mechanism and constraint

3.5.2 Function as a constraint on mechanism

Summary

Further reading