The field of insect immunity has made enormous progress in describing the basic molecular mechanisms of the immune response to microbes. This work not only told us how insects work but also how the human innate immune system works, because many of the basic mechanisms are conserved between these two organisms. Three serious problems remain in our description of innate immunity. The first stems from our basic definition of the process; innate immune systems are defined as responding to threats using germ-line-encoded receptors. This is in contrast to a so-called adaptive immune system, which can increase the specificity of its detectors and effectors through somatic recombination and mutation. Often one is given the impression that an innate immune response is static and stereotypical, producing the exact same molecular output every time it encounters an elicitor. Nothing could be further from the truth; innate immune responses are supple and responsive. Innate immunity fluctuates with changes in the native microbiota, energy availability, feeding, circadian rhythm, age, and even past exposure to microbes. Sometimes it is surprising that we can even get experiments to repeat, given the responsiveness of the insect.
A second problem with our description of innate immunity is that this subject has become a victim of its own success. Past work focused on the molecular mechanisms behind elicitor recognition and the signalling pathways regulating initial transcription events. As this generated excitement in the larger world of vertebrate immunology it further focused our attention on these molecular studies. Unfortunately, however, we still don't know why most insects die when they are infected with a pathogen, yet this type of knowledge is critical if insects are to be used as a model for disease or even if we are to simply understand the physiological regulation of immunity.
Third, we tend to describe the immune response of insects very simply. However, ecological studies of plant-herbivore interactions predict that hosts evolve two methods of retaining fitness when faced with a predator; they can increase either their resistance or their tolerance of the threat. Resistance is defined as the inverse of the herbivore intensity. Tolerance is the reaction norm found when the fitness of the plant is plotted at different herbivore levels. In tolerant plant strains the slope of this tolerance curve is shallow, indicating that the plants do not suffer a large loss in fitness as herbivore levels increase. Together these two properties comprise the defensive capabilities of a host. In insect studies, we have focused most of our attention on resistance and have largely ignored tolerance. However, tolerance has been shown to play a role in insect immunity and measurements of tolerance need to be taken in future experiments (Corby-Harris et al., 2007; Ayres et al., 2008).
To understand how insect immunity is regulated we need to study the interactions of all those aspects of physiology that impact immunity. This includes both resistance and tolerance aspects of defence as well as all of the other assorted physiological systems of the insect that alter the immune response.
Our hypothesis is that an insect's innate immune response sits in the centre of a physiological net and the immune response is sensitive to changes throughout this net. The goal of this chapter is to try to tie all of these physiological strands together and demonstrate how innate immunity alters the gross physiology of an insect and how the gross physiology, in turn, alters the immune response. An emergent property that falls out of this analysis is the prediction of several types of physiological collapse; these collapses result from positive-feedback loops that lead to amplified and damage-inducing immune/physiological responses.
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