The Quarterly Review of Biology INTEGRATING HISTORICAL AND MECHANISTIC BIOLOGY ENHANCES THE STUDY OF ADAPTATION

Adding a causal, mechanistic dimension to the study of character evolution will increase the strength of inferences regarding the evolutionary history of characters and their adaptive consequences. This approach has the advantage of illuminating mechanism and testing evolutionary hypotheses rigorously. We consider the advantages of combining mechanistic and historical biology in the study of behavior, physiology, and development. We present six examples to illustrate the advantages: (1) preexisting biases in sound perception in frogs; (2) preexisting biases in visual cues in swordtail 384 Volume 77 THE QUARTERLY REVIEW OF BIOLOGY fishes; (3) exploitation of prey location behavior for attraction of mates in water mites; (4) heterospecific mating in asexual molly fishes; (5) developmental foundation of morphological diversification in amphibian digits; and (6) locomotor performance at low temperature and the evolution of nocturnality in geckos. In each of these examples, the dominant role of history, combined with organismal integration, makes ignoring history a risky proposition. U HOW LIFE works is the fundamental goal of biology. As modern biologists, we strive for a mechanistic explanation of phenomena that range from molecules to ecosystems. Mechanistic understanding involves distinguishing reproducible and testable causal patterns from noncausal or nontestable associations (Brandon 1996). With the advent of objective methods for generating and testing hypotheses of phylogenetic relationships (Hennig 1966), researchers actively began to incorporate phylogenetic perspectives into many areas of biological research focused on mechanistic understanding, including (as general examples) behavior, life history, functional and developmental morphology, and comparative physiology (Lauder 1982, 1990, 1991; Stearns 1992; Arnold 1993, 1994b; Niewiarowski 2001). This has meant that these and other fields, long isolated from systematic biology, gained historical perspective that has enriched interpretations, sometimes opening new pathways for understanding how history and biological mechanisms interact (e.g., Galis 1996). On the one hand, there has been enthusiastic integration of historical perspectives with mechanistic biology, as attested by a large literature that includes numerous symposia volumes (e.g., Harvey et al. 1996), collections of essays (e.g., Martins 1996), book chapters (e.g., Lauder 1991), and monographs (e.g., Brooks and McLennan 1991; Harvey and Pagel 1991; Garland and Carter 1994; Feder et al. 2000), in addition to a large number of research papers. On the other hand, authors have argued that the new methods are fundamentally a distraction, and that they obscure the central issues in fields such as behavioral evolution (Reeve and Sherman 1993, 2001) and comparative physiology (Mangum and Hochachka 1998). Our objective in this paper is to illuminate how intricately history and mechanism are integrated, and to show the value of a phylogenetic perspective in understanding patterns of evolution in behavior, morphology, and physiology. We present case studies that show how historical perspectives enable better understanding of mechanisms. We also argue that deep understanding of history and mechanism is invaluable for interpretation of results that otherwise could be seen as the workings of some ongoing dynamic (Ghiselin 1999). In particular we wish to counter the view that adequate understanding of complex patterns of evolution can be obtained by using an approach that relies solely on surrogates or proxies for fitness, such as performance or appearance, instead of the underlying and we believe more significant biological features of organisms. In the following sections, we begin first by defining mechanism and history. Second, we present a logical treatment of the conflict that exists between integrative (historical, mechanistic) and purely adaptive approaches. Testability is a major advantage of the integrative approach we advocate. Next, we outline a protocol for testing integrative hypotheses and show how purely adaptive explanations are not scientifically valid unless the integrative explanation is first shown to be false. We use six examples from behavior, development, and physiology to illustrate the power and necessity of an integrative approach in the study of complex integrated systems. Mechanism and History Since mechanistic and historical biology are central concepts in our argument, we define what we mean by mechanism and history, and show how they can be integrated in answering evolutionary questions. Mechanism and history can be thought of as two dimensions or axes (Autumn et al. 1999) that each contain important information, but by themselves may be insufficient to address evolutionary questions involving complex integrated systems. We use “mechanism” broadly to mean experimentally established, testable, causal December 2002 385 HISTORICAL AND MECHANISTIC BIOLOGY relationships among parts (Lauder 1991; Brandon 1996). The appropriate level or levels in the biological hierarchy for a mechanistic explanation will depend on the question ( Jacob 1977). Since causal interactions may occur in both upward (small to large) and downward (large to small) directions (Bock 1989; Autumn 1995; Brandon 1996), it is not always possible to reduce the function of organisms to simple molecular causes (Savageau 1991). For this reason, mechanisms describe interactions that range from molecules to ecosystems. Figure 1A shows a simple mechanism consisting of a lever arm, gears, and a belt. Each part of the mechanism is related causally to the production of torque, the measure of performance in this example. Variation in torque is a mechanistic consequence of variation in the moment arm and variation in the gear ratio. Let us imagine that there are two versions of this mechanism: A and B. A and B are similar in all respects except that one of the gears in B is larger than in A. Is the larger gear in B an adaptation for increasing torque? If the parts of A and B were laid out randomly on a table, there would be no way to predict whether a larger gear would increase torque because the order of gears in the mechanism will determine if increasing gear size increases or decreases torque. By adding information on how the mechanism is put together and how it works, one can predict the effects of a larger gear with a great deal of certainty. The strength of the prediction will depend on the strength of experimental and theoretical support for the mechanism in question. In this example, the causal effect of variation in the form of each part can be predicted by the equation: Torque Moment Arm Size of Gear