Chapter 1 Introduction and Historical Perspective “ Nothing in biology makes sense except in the light of evolution. ” modified by the developmental history of the organism, Theodosius Dobzhansky its physiology – from cellular to systems levels – and by the social and physical environment. Finally, behaviors are shaped through evolutionary forces of natural selection OVERVIEW that optimize survival and reproduction ( Figure 1.1 ). Truly, the study of behavior provides us with a window through Behavioral genetics aims to understand the genetic which we can view much of biology. mechanisms that enable the nervous system to direct Understanding behaviors requires a multidisciplinary appropriate interactions between organisms and their perspective, with regulation of gene expression at its core. social and physical environments. Early scientific The emerging field of behavioral genetics is still taking explorations of animal behavior defined the fields shape and its boundaries are still being defined. Behavioral of experimental psychology and classical ethology. genetics has evolved through the merger of experimental Behavioral genetics has emerged as an interdisciplin- psychology and classical ethology with evolutionary biol- ary science at the interface of experimental psychology, ogy and genetics, and also incorporates aspects of neuro- classical ethology, genetics, and neuroscience. This science ( Figure 1.2 ). To gain a perspective on the current chapter provides a brief overview of the emergence of definition of this field, it is helpful to survey some of the his- experimental psychology and ethology, followed by a torical milestones of experimental psychology and the study historical perspective of how concepts of natural selec- of animal behavior, together with the development of the tion and principles of heredity were combined by the concept of evolution through natural selection and its coales- founders of the modern evolutionary synthesis into cence with Mendel’s principles of heredity, which gave rise the sciences of population and quantitative genetics. to the fields of quantitative and population genetics. These Subsequently, population genetic, quantitative genetic are the critical cornerstones of today’s behavioral genetics. and molecular genetic principles could be applied to In the following sections we will provide broad overviews experimental psychology, behavioral ecology, and of the development of each of these disciplines to show, at behavioral neuroscience, to give rise to the modern the end of this chapter, how they can be brought together to field of behavioral genetics. We will highlight some of study the link between genes, brain, and behavior. the major historical milestones and controversies. We indicate how the past history of the field has laid the foundation for examining the genetic architectures of Experimental Psychology and Animal behaviors in the genomic era. This historical perspec- Behavior tive provides an important reference frame for under- standing past, current, and future trends and issues in Since time immemorial philosophers and naturalists have behavioral genetics. been intrigued by animal behaviors. Twenty-three centu- ries ago Xenophon, a disciple of Socrates, wrote a treatise on The Art of Horsemanship which covers basic aspects of horse husbandry and training, while paying great attention THE RISE OF THE MODERN FIELD to their behaviors. Studies on animal behavior, however, OF BEHAVIORAL GENETICS remained descriptive and anthropocentric (interpreted in terms of human experience) for much of recorded his- Behaviors are mediated by the nervous system in response tory. Human emotions and cultural values were projected to environmental conditions. From a genetics perspective, onto animals, some of which were considered intrinsically behaviors are complex traits determined by networks of noble (lions, horses), loyal (dogs), or repugnant (snakes), multiple segregating genes that are influenced by the envi- and discussions on the relative intelligence of species gen- ronment. Both genetic factors and neural circuits can be erated fruitless debates. R. Anholt and T. Mackay: Principles of Behavioral Genetics Copyright © 2010 Elsevier Inc ISBN: 978-0-12-372575-2 1 All rights Reserved 005_P372575_Ch01.indd5_P372575_Ch01.indd 1 88/22/2009/22/2009 110:09:280:09:28 AAMM 2 Principles of Behavioral Genetics FIGURE 1.1 A schematic representation of the Evolution scope of behavioral genetics. Both developmental and physiological factors modify gene expression, neural circuits, and interactions between them as they mediate the expression of an appropriate behavior. Interactions with the physical and social environment provide feedback information that can alter gene expression and neural circuitry to modify expression of the behavior, again in the context of Genes the organism’s physiology and development. The behavior itself becomes an instrument of evolution that acts on the genome through changes in allele Development Physiology frequencies under the forces of natural selection. Nervous system Social Environmental interactions interactions Behavior Lorenz Thorndike von Frisch Pavlov Skinner Tinbergen Experimental psychology/ethology Benzer Hirsch Lamarck Darwin Galton Pearson Fisher Haldane Evolution Wright Dobzhansky Behavioral genetics Modern evolutionary Mendel Miescher Morgan synthesis Capecchi Mullins Watson Evans Axel Correns Sanger Genetics Crick Nierenberg Smithies Buck von Tschermak de Vries Avery McClintock Temin McLeod Kandel McCarty Hodgkin Cole Huxley Hubel Loewi Dale Katz Wiesel Neuroscience 19th century 20th century 21th century FIGURE 1.2 Historic time course of the convergence of experimental psychology, ethology, evolution, genetics, and neuroscience to enable the multi- disciplinary study of genes, brain, and behavior through behavioral genetics. A sampling of names of pioneers who made seminal discoveries and who will be mentioned later in this chapter is indicated. Note that this list is not exhaustive. Studies in which a behavior could be modified in a would salivate in anticipation of food. He found that he predictable manner and subjected to scientific scrutiny could elicit this salivation response reliably by administering did not begin in earnest until the end of the nineteenth and a distinct auditory or visual stimulus that would signal antic- beginning of the twentieth century, when a Russian ipation of a subsequent food reward. Although it is generally scientist, Ivan Pavlov, living in Leningrad, studied gas- believed that Pavlov rang a bell when training his dogs, his tric function in dogs by analyzing their salivary secretions writings do not mention a bell, but rather whistles, metro- in response to food ( Figure 1.3 ). Pavlov noticed that dogs nomes, tuning forks, and a variety of other stimuli (no bell 005_P372575_Ch01.indd5_P372575_Ch01.indd 2 88/22/2009/22/2009 110:09:290:09:29 AAMM Chapter | 1 Introduction and Historical Perspective 3 FIGURE 1.3 Ivan Pavlov (left); one of Pavlov’s dogs (right) pre- served in the Pavlov Museum. FIGURE 1.4 A typical “ Skinner ” box in which a pigeon learns that it will receive a food grain reward when it pecks on a spot of bright light. was found in his carefully-preserved laboratory after his American scientist Burrhus Frederic Skinner, who devel- death in 1936). Pavlov called the responses of his dogs ’ oped the paradigm of operant conditioning as a con- conditional reflexes , now generally referred to as classical trast to the classical conditioning experiments of Pavlov. conditioning or associative learning . His observations are Operant conditioning results in behavioral modification reminiscent of Aristotle’s assessment that “ When two things through positive reinforcement. Skinner’s favorite ani- commonly occur together, the appearance of one will bring mal, which remains a model for experimental psycholo- the other to mind. ” Pavlov’s studies heralded the birth of gists today, was the pigeon ( Figure 1.4 ). Skinner reasoned experimental and comparative psychology. that when a hungry pigeon would receive a food reward, it Intrigued by the debate about whether animals have might associate the food with the execution of a particu- innate intelligence or develop responses by trial and error, lar behavior and repeat that behavior. Skinner observed Edward Thorndike, an American scientist and contempo- that pigeons would repeat behaviors they had exhibited rary of Pavlov, conducted experiments in which he mea- by chance when food rewards were delivered at random. sured the time it would take for cats to escape from a In his article “ Superstition ” in the Pigeon , Skinner wrote puzzle box. He constructed learning curves that showed “ One bird was conditioned to turn counter-clockwise about that cats do not have an innate understanding, but rather the cage, making two or three turns between reinforce- learn gradually through trial and error in which each pre- ments. Another repeatedly thrust its head into one of the vious success improves performance in a subsequent trial. upper corners of the cage. A third developed a “ tossing ” In his 1911 book Animal Intelligence Thorndike lambasted response, as if placing its head beneath an invisible bar prevailing notions of animal intelligence of his time: “ In and lifting it repeatedly. Two birds developed a pendu- the first place, most of the books do not give us a psychol- lum motion of the head and body, in which the head was ogy, but rather a eulogy of animals. They have