Optimization Theory in Evolution

In recent years there has been a growing attempt to use mathematical methods borrowed from engineering and economics in interpreting the diversity of life. It is assumed that evolution has occurred by natural selection, and hence that complex structures and behaviors are to be interpreted in terms of the contribution they make to the survival and reproduction of their possessors-that is, to Darwinian fitness. There is nothing particularly new in this logic, which is also the basis of functional anatomy, and indeed of much physiology and molecular biology. It was followed by Darwin himself in his studies of climbing and insectivorous plants, of fertilization mechanisms and devices to ensure cross-pollination. What is new is the use of mathematical techniques such as control theory, dynamic programming, and the theory of games to generate a priori hypotheses, and the application of the method to behaviors and life history strategies. This change in method has led to the criticism (e.g. 54, 55) that the basic hypothesis of adaptation is untestable and therefore unscientific, and that the whole program of functional explanation through optimization has become a test of ingenuity rather than an enquiry into truth. Related to this is the criticism that there is no theoretical justification for any maximization principles in biology, and therefore that optimiza­ tion is no substitute for an adequate genetic model. My aim in this ' review is not to summarize the most important conclusions reached by optimization methods, but to discuss the methodology of the program and the criticisms that have been made of it. In doing so, I have taken as my starting point two articles by Lewontin (54, 55). I disagree with some of the views he expresses, but I believe that the development of evolution theory could benefit if workers in optimization paid serious attention to his criticisms. I first outline the basic structure of optimization arguments, illustrating this with three examples, namely the sex ratio, the locomotion of mammals, and foraging behavior. I then discuss the possibility that some variation may be selectively neutral, and some structures maladaptive. I summarize and comment on criticisms made by Lewontin. The most damaging undoubtedly is the difficulty of testing the