Chimeras and Consciousness: Evolution of the Sensory Self

17. Origins of the Immune System

17 Origins of the Immune System Margaret J. McFall-Ngai Evolution in crowded environments leads to surprising developments. Here McFall-Ngai argues for the striking idea that even the vertebrate immune system may be an organ of symbiosis. Over the eons, animals, plants, and all other multicellular eukaryotes diversified within the context of a bacteria-rich environment. (See plate XII.) Evolutionary selection pressure was exerted by prokaryotic and other microbes on larger organisms, especially animals. These organisms had to sense and respond to biotic cues and stimuli in marine settings steeped with life. In animals, a complicated reaction to the biotic world involves the activation of a multifaceted immune system. The vertebrate immune system evolved in the presence of bacteria that were sensed, responded to, and integrated into it. As most animals are digestive tubes—from mouths through stomachs and intestines to anuses, covered by integument such as skin—the animal immune system probably evolved, in my view, from the exigency of distinguishing healthy necessary bacterial inhabitants of these tubes and coverings relative to opportunistic , potentially dangerous hungry exploiters. Although animals possess both types of coevolved partners—those in symbiotrophic symbioses and those that are potential threats in necrotrophic associations— the vertebrate immune system mainly evolved from bacterial interactions that nurture or tend to destroy physiological homeostasis (often syntrophies ) of co-evolved animal-microbial partnerships. Our concepts of animal biology change rapidly when we recognize that the animal kingdom comprises far more than single types of eukaryotic cells. More accurately, it comprises the interconnected, coevolving sets of communities with one principal eukaryotic cell type and often more than several hundred distinct kinds of bacteria. The findings that the integumentary (skin) and the digestive systems of the average human body harbor a 200 Chapter 17 coevolved consortium of 1011 skin bacteria and 1014 digestive bacteria demand that biologists reconsider their most basic concepts of the physiology of these systems. Perhaps the most obvious and dramatic changes will be seen in our view of the form and function of the immune system, as a principal response to the biotic environment. The growing appreciation of the true nature of animals renders obsolete the traditional idea of the immune system as a “non-self” recognition system. Most notably, humans require the partnerships of many different kinds of bacteria (phylotypes) for normal growth, development, and homeostasis. Our understanding of the immune system must be expanded to include these new findings. Let us step back and reconsider the function of the immune system in light of related basic biological principles. What similarities and differences exist in the ways animals respond to physical, chemical, and biological environmental stimuli? The primary purview of the animal nervous system is to modulate activity in response to abiotic, or physical changes. Three major types of neurons carry out this task: sensory neurons, interneurons, and motor neurons. Sensory neurons act as transducers of the environmental information (e.g., changes in light, changes in temperature, mechanical stimuli) and convert it into a usable form. The interneurons integrate the input so that an eventual appropriate response is made. The response or output is the job of the motor neurons, which mediate the activity of the effectors (e.g., muscles, chromatophores, bioluminescent organs). Of course, much of the information carried by these abiotic forces provides the animal with knowledge about the state of the biotic world, such as the presence of predators or prey, competitors, and food. Animals use light to respond to the biotic world (e.g., predators, prey, mates, young, fruits, seeds). In the big picture, perhaps light is secondary for all five kingdoms, but it is crucial to invertebrate and vertebrate animals as a response to other living creatures and their products released into the environment. The same might be said for temperature among communal vertebrates. The immune system seems to respond to antigens, to biotic products of metabolism, and to prokaryotes. The immune systems of animals also have sensors, integrators, and effectors that respond to interactions with citizens of the microbial world. The emphasis of study has been on microbial pathogenesis (necrotrophy). The most widely held belief is that the immune system views microbes as germs sensed by certain animal cells. The information would be integrated in such a way that the entire animal responds to rid Origins of the Immune System 201 its body of the encroaching dangerous microbe. This viewpoint changes with our increasing awareness of...