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1. Adaptation and the Evolution of Physiological Characters Bennett, A. F. 1997. Adaptation and the evolution of physiological characters, pp. 3-16. In: Handbook of Physiology, Sect. 13: Comparative Physiology. W. H. Dantzler, ed. Oxford Univ. Press, New York. 1. Adaptation and the evolution of physiological characters Department of Ecology and Evolutionary Biology, University of California, ALBERT F. BENNETT 1 Irvine, California among the biological sciences (for example, behavioral CHAPTER CONTENTS science [I241). The Many meanings of "Adaptationn In general, comparative physiologists have been Criticisms of Adaptive Interpretations much more successful in, and have devoted much more Alternatives to Adaptive Explanations energy to, pursuing the former rather than the latter Historical inheritance goal (37). Most of this Handbook is devoted to an Developmentai pattern and constraint Physical and biomechanical correlation examination of mechanism-how various physiologi- Phenotypic size correlation cal systems function in various animals. Such compara- Genetic correlations tive studies are usually interpreted within a specific Chance fixation evolutionary context, that of adaptation. That is, or- Studying the Evolution of Physiological Characters ganisms are asserted to be designed in the ways they Macroevolutionary studies Microevolutionary studies are and to function in the ways they do because of Incorporating an Evolutionary Perspective into Physiological Studies natural selection which results in evolutionary change. The principal textbooks in the field (for example, refs. 33, 52, 102, 115) make explicit reference in their titles to the importance of adaptation to comparative COMPARATIVE PHYSIOLOGISTS HAVE TWO GOALS. The physiology, as did the last comparative section of this first is to explain mechanism, the study of how organ- Handbook (32). Adaptive evolutionary explanations isms are built functionally, "how animals work" (113). are woven throughout the fabric of the science. Studies of this type are undertaken at a variety of However, the assumption that adaptation is the sole organizational levels: organismal, organ system, organ, explanation for natural diversity in living systems has tissue, cell, or molecular and biochemical. Ideally, a been called into question (54, 80, 81, 82, 132, 133) study will span several of these, integrating information and has become a point of contention among many from lower to higher levels and illuminating mecha- organismal and evolutionary biologists. The rote appli- nisms from higher to lower. The second goal is to cation of adaptive explanations for all physiological explain the diversity of functional systems found phenomena has effectively uncoupled comparative among organisms. In contrast to "how" questions, this (ecological) physiology from evolutionary biology. goal attempts to answer "why" questions: Why is an Evolutionary biologists generally ignore and are igno- organism built the way it is and why does it function rant of comparative physiology. Their courses do not in a particular way and not in another? How and why discuss the evolution of physiological characters, and do physiological properties change through time? major textbooks in evolution (for example, ref. 43) The first goal entails equilibrium (in Lauder's sense contain virtually no reference to physiological phenom- [74])studies-that is, those which examine the present- ena. Comparative physiology should be a field central day associations among characters and do not under- to evolutionary biology, given the importance of the take causal (in the sense of historical) explanations. In functional characters that it studies and its avowed contrast, the second goal requires transformational or evolutionary orientation. If comparative physiology is evolutionary, explanations and hence must deal, at to make a serious contribution to evolutionary biologj., least implicitly, with the ecology, genetics, and history it must rethink its historical commitment to adapta- of the organism and its population. For both goals, a tionism. primary reference point is the function of an organism An increasing number of studies have tested alterna- In its natural environment. These goals are not unique tives to adaptive explanations and examined the evolu- to comparative physiology; they are broadly shared tion of functional and structural characters. A diversity 4 HANDBOOK OF PHYSIOLOGY-COMPARATIVE PHYSIOLOGY of approaches is now available for the study of the be the state of having become familiar with surround- evolution of physiological traits and mechanisms. ings. This usage is colloquial, as in permitting an ani- Comparative physiologists are now almost uniquely mal to adapt to experimental conditions. It usually positioned to utilize these approaches to understand refers to placing an organism in an apparatus or envi- how important functional characters have changed and ronment prior to beginning experimental measure- may change through time. The types of organismal ments to minimize fright or activity. (4) Adaptation can character that interest comparative (ecological) physi- be a functional change in an organism after exposure ologists (for example, energy exchange, thermoregula- to new conditions or a new environment. Organisms tion, and locomotor performance) are precisely those frequently reorganize their physiological systems, par- that everyone expects will be of importance to fitness ticularly their rate processes, in response to changed and evolutionary success. Such studies must test (and conditions. The most familiar of these responses is not assume) the role of adaptation in shaping those temperature adaptation (acclimation or acclimatiza- characters. tion), but the term is also used to describe alteration of The purpose of this chapter is to examine what we muscle structure and function to altered stress patterns, know about the evolution of physiological systems and changes in osmotic and ionic regulation in different the role of adaptation in shaping them. First, the several environmental media, etc. The term applies to such meanings of the term "adaptation" for physiologists changes in both laboratory and natural conditions. are explored and their relevance to character evolution The documentation and physiological basis of such discussed. Then, alternatives to, or constraints on, ad- plasticity is a particularly popular area of physiological aptation are examined. Methods for the study of the study (61, 100). (5) Adaptation can be the process of evolution of physiological characters in both the field improvement of fitness in a population of organisms and the laboratory are then discussed, as well as their in response to natural selection. This sense refers to importance to future directions in comparative physi- the Darwinian evolutionary process, and it is in this ology. sense that most evolutionary biologists use the term. It assumes that individuals with characteristics favored in their particular environment will reproduce more THE MANY MEANINGS OF "ADAPTATION" and that the favored characters will increase in fre- quency over generations. The literature in evolutionary Physiologists and other organismal biologists employ biology dealing with the intricacies of this concept is the term "adaptation" to describe an especially wide large (readers are referred to the following books and variety of different biological responses, only some of articles for a more comprehensive discussion of evolu- which actually refer to evolutionary phenomena. Many tionary adaptation: 7, 16-18, 81, 87, 89, 94, 104, of these uses are not widely shared with, or understood 122, 132). (6) Adaptation can involve a character that by, other biologists, a situation that easily may lead to originated due to natural selection. This usage refers confusion and misunderstanding. This section clarifies to a structure or function that is the product of the the multitude of uses and definitions of this word. preceding process. In this sense, a nasal salt gland A physiologist or organismal biologist might well may be an adaptation resulting from the process of use adaptation in any of the following senses: (1) adaptation (definition 5) to a saline environment. (7) Adaptation can be the alteration of a sensory or ner- Adaptation can involve a preexisting character that is vous response under constant stimulus. The rate of beneficial to an organism in a particular environment firing of sensory cells or neurons usually changes or circumstance. The distinction between this and the acutely with the onset or offset of a stimulus. If that previous definition is whether the character has been a stimulus is maintained, the response may either de- target for selection in the current environment or is a crease, as in pressure sensation, or increase over time, feature that is adventitiously useful. Preadaptation, as in dark accommodation. Both are termed adapta- protoadaptation (44), and exaptation (55) connote an- tion. (2) Adaptation can be a syndrome of physiological cestral features previously acquired that find a new responses to environmental stress. Specifically, this us- utility in new circumstances. (8) Adaptation can in- age refers to the General Adaptation Syndrome (116) volve a generally and phylogenetically widespread in vertebrates, in which a variety of stressors may structure or function necessary for, or promoting, sur- activate release of adrenal hormones with widespread vival, a feature of many living systems, sometimes physiological effects, including raising blood pressure, crucial for
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