Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments

11. Behavior in Neurobiology

263 11 BEHAVIOR AND NEUROBIOLOGY Justin S. Rhodes and Tadeusz J. Kawecki BEHAVIOR EVOLVES FIRST THE EVOLUTION OF BEHAVIOR EXPERIMENTAL METHODS Artificial Selection Mass Selection Laboratory Natural Selection Methodological Considerations in Evolutionary Experiments Line-Cross Analysis Gene Mapping: New Technology Genetic Engineering EXAMPLES OF CORRELATED RESPONSES TO SELECTION ON BEHAVIOR THE EVOLUTION OF MATING SYSTEMS IN VOLES: FROM GENES TO BEHAVIOR TESTING ADAPTIVE HYPOTHESES RELEVANCE FOR PUBLIC HEALTH CONCLUSIONS AND FUTURE DIRECTIONS Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments, edited by Theodore Garland, Jr., and Michael R. Rose. Copyright © by the Regents of the University of California. All rights of reproduction in any form reserved. The tree of life is decorated with an extraordinary diversity of animal behavior (figure 11.1). Such behaviors as foraging, reproducing, moving through the environment, and avoiding predators are all clearly major determinants of survival and reproductive success and hence are thought to be under relatively strong natural and sexual selection. Although some behaviors are culturally transmitted, the vast majority evolve by genetic mechanisms . One of the earliest pieces of direct evidence that behavior can be shaped by evolutionary processes was domestication of wolves into dogs, which is thought to have 264 • L E V E L S O F O B S E R V A T I O N FIGURE 11.1 Massive behavioral diversity in feeding and home range size among vertebrate species. Some species stalk, attack, and kill other animals for food (A), whereas others forage entirely on plant material (B). Among the predators, some sit and wait for their prey to come to them (C), whereas others actively pursue their prey (D). Some animals spend their entire life within few square meters of space (E), whereas others roam for miles in the open ocean (F). Presumably these behavioral shifts are mediated by changes in the brain that evolved through structural modifications of the genome. occurred as far back as fifteen thousand years ago (Savolainen et al. 2002). Since then, a variety of animals have been domesticated, thus providing ample evidence that selective breeding can alter behavior (see also Barnett and Smart 1975; Simões et al. this volume). Domestication also demonstrates that genes can influence behavior and that behavior can evolve rapidly (Garland 2003; Greenspan 2003; Robinson 2004). In recent decades, a number of natural genetic polymorphisms that affect behavior have been identified, and some progress has been made toward understanding how changes in DNA alter gene expression and/or protein structure, nervous system development, and neural physiology to produce differences in behavior (Ross and Keller 1998; Keller and Parker 2002; Greenspan 2004; Fitzpatrick et al. 2005). Selection experiments and experimental evolution approaches offer powerful tools for elucidating the origin and mechanisms of behavioral diversity. The discipline is useful to establish basic knowledge about nature, but it also has powerful applications for biomedicine. For example, advances in understanding how genes influence behavior could provide insights into the etiology of drug addiction, obesity, or attention-deficit/ hyperactivity disorder (ADHD) (Rhodes et al. 2005). Here, we review some of the methods in experimental evolution that can be used to study the evolution of behavior (see also Fry this volume; Swallow et al. this volume; Zera and Harshman this volume). We illustrate how these methods can be applied toward understanding the origin and mechanisms of behavioral diversity using examples from our own work and from the literature. BEHAVIOR EVOLVES FIRST A long-standing idea in evolutionary biology is that “behavior evolves first” (Mayr 1958; Blomberg et al. 2003). For example, natural selection will only favor physiological adaptations to a novel host plant species in herbivorous insects after the females have begun utilizing the new host for oviposition. Similarly, before the ancestors of whales evolved fins, they probably evolved a brain that made them want to spend time in the water. Providing support for this idea are fossil whales without fins (Gingerich et al. 2001) and living species that display evidence of a recent behavioral transition but without corresponding morphological adaptations (Fryer and Iles 1972). For example, the speciose family of freshwater tropical fish, cichlids, display an extraordinary diversity in feeding habits with clear evidence for genetic adaptations in dentition (Ruber and Adams 2001). However, a few species show no evidence for specialized dentition. Cyrtocara moorii, for instance, has large, irregularly shaped teeth that are inserted on the jaws in an uneven fashion. This cichlid feeds on food particles stirred...