Anais da Academia Brasileira de Ciências ISSN: 0001-3765 [email protected] Academia Brasileira de Ciências Brasil Marler, Peter Innateness and the instinct to learn Anais da Academia Brasileira de Ciências, vol. 76, núm. 2, june, 2004, pp. 189-200 Academia Brasileira de Ciências Rio de Janeiro, Brasil Disponible en: http://www.redalyc.org/articulo.oa?id=32776202 Cómo citar el artículo Número completo Sistema de Información Científica Más información del artículo Red de Revistas Científicas de América Latina, el Caribe, España y Portugal Página de la revista en redalyc.org Proyecto académico sin fines de lucro, desarrollado bajo la iniciativa de acceso abierto Anais da Academia Brasileira de Ciências (2004) 76(2): 189-200 (Annals of the Brazilian Academy of Sciences) ISSN 0001-3765 www.scielo.br/aabc Innateness and the instinct to learn PETER MARLER Animal Communication Laboratory, Department of Neurobiology, Physiology and Behavior University of California, Davis, CA 95616, USA Manuscript received on January 15, 2004; accepted for publication on February 5, 2004. ABSTRACT Concepts of innateness were at the heart of Darwin’s approach to behavior and central to the ethological theorizing of Lorenz and, at least to start with, of Tinbergen. Then Tinbergen did an about face, and for some twenty years the term ‘innate’ became highly suspect. He attributed the change to Lehrman’s famous 1953 critique in which he asserted that classifying behaviors as innate tells us nothing about how they develop. Although Lehrman made many valid points, I will argue that this exchange also led to profound misunderstandings that were ultimately damaging to progress in research on the development of behavior. The concept of ‘instincts to learn’, receiving renewed support from current theorizing among geneticists about phenotypic plasticity, provides a potential resolution of some of the controversies that Lehrman created. Bioacoustical studies, particularly on song learning in birds, serve both to confirm some of Lehrman’s anxieties about the term ‘innate’, but also to make a case that he threw out the genetic baby with the bathwater. The breathtaking progress in molecular and developmental genetics has prepared the way for a fuller understanding of the complexities underlying even the simplest notions of innate behavior, necessary before we can begin to comprehend the ontogeny of behavior. Key words: innateness, song learning, phenotypic plasticity, behavioral genetics, Tinbergen’s four questions. INTRODUCTION I have been most intimately involved, vocal commu- nication in birds, and the development of birdsong. One of the great issues that have long confronted biologists, philosophers, and social scientists is the HISTORICAL BACKGROUND controversy about nature and nurture. To what ex- tent are we products of our genetic make-up, and I was lucky, as a student, to be present at the very be- to what extent are we reflections of the cumulative ginning of birdsong studies, and to participate in the consequences of the myriad of experiences over a initial spread of ethology, first in Europe, and then lifetime? In our own case this is a conundrum that in America. These were exciting times in the early we will never solve, but with animals we may have 1950s, when so much about the study of behavior some chance of gaining at least a rough understand- was in a state of ferment, much of it triggered by the ing of the principles involved. It has been a central contributions of Konrad Lorenz (Fig. 1). issue in the study of animal behavior for a long time, Many new directions were emerging, summa- especially in that aspect of bioacoustics with which rized in Tinbergen’s list of issues to be addressed, outlined by him for me as external examiner on E-mail: [email protected] my PhD thesis committee. Interestingly he was An Acad Bras Cienc (2004) 76 (2) 190 PETER MARLER not alone in trying to forecast the future. Julian Huxley, acknowledged as an influential colleague by Lorenz, (Fig. 1) wrote an appreciative piece called ‘Lorenzian ethology’, with a list similar to Tinber- gen’s (Huxley 1963). The two of them shared the same three main points of focus: (1) the causation of behavior, by which they meant the underlying physiological machinery; (2) the survival value of behavior; and (3) its role in evolution. In the years that followed, there has been dramatic progress in all three of these areas, and research in bioacoustics has made major contributions in all of them rang- ing from insects (e.g. Otte 1977, Michelsen and Larsen 1983, Michelsen 1992, Bennet-Clark 1989, 1998, 1999) to anurans (e.g. Ryan 1985, Wilczyn- ski and Ryan 1999, Schwartz 2001, Gerhardt and Huber 2002), birds (Thorpe 1961, Kroodsma and Miller 1982, 1996, Catchpole and Slater 1995) and mammals (Eisenberg 1976, Gould 1983, Cheney and Seyfarth 1990). But Tinbergen chose to add a fourth area, the development of behavior (Tinbergen 1963), which was destined to become something of an orphan. Even today we have no comprehen- sive theory of behavioral ontogeny. I have spent much time trying to understand why it happened that progress in the study of development was the slow- est of the four areas of study. In doing so, I have gone back repeatedly to other events taking place in the behavioral sciences in the fifties, many of them Fig. 1 – Six key figures in the innateness controversy: Lorenz, directly provoked by the renewed interest in Tinbergen, Heinroth, Huxley, Lehrman, and Hebb. instinctive behavior. That is the theme that I want to present here. but his teachers took the view that behavior was too The Concept of Innateness variable and amorphous to be amenable to the same Lorenz, Tinbergen, and my own teacher and men- kind of study. But with the encouragement of his tor, W.H. Thorpe, like Darwin, were all fully con- most influential mentor, Oscar Heinroth (Fig. 1), vinced of the value of the concept of in- Lorenz became convinced that ethology could be as stinct, defined by Webster’s dictionary as ‘‘an in- objective as comparative anatomy. As director of the born tendency to behave in a way characteristic of Berlin Zoo, Heinroth was intimate with the behav- a species’’. As a medical student in Vienna, Lorenz ior of scores of animals, many of which he raised in was exposed to the ferment of phylogenetic theo- captivity, often by hand, especially birds. His mon- rizing in comparative anatomy and morphology, umental ‘Die Vögel Mitteleuropas’, written with his mostly based on the study of bones and skeletons. wife, Magdalena Heinroth, is full of details, richly The young Lorenz was more interested in behavior, illustrated, about the development of behavior in an An Acad Bras Cienc (2004) 76 (2) INNATENESS AND THE INSTINCT TO LEARN 191 amazing number of birds (Heinroth and Heinroth Tinbergen became much more cautious about using 1924-1933). Among Lorenz’s zoo favorites were the term ‘innate’, and he was joined by other lead- waterfowl, and watching them he found that many ing ethologists, including Patrick Bateson, Robert of the distinctive, species-specific displays they per- Hinde, and Gerard Baerends, and many other in- formed in captivity matched those in the wild, even fluential figures. As a consequence, the very fun- though they had no adult tutors to instruct them. dament on which the ethological approach to the In his 1941 monograph on duck behavior, Lorenz development of behavior was founded suddenly be- compared in detail 20 species, all of whose dis- came suspect. In the years that followed, the term plays appeared to him to develop normally in cap- ‘innate’ became a forbidden word. And of course tivity, down to the finest details of nod-swimming the message was not lost on students who, like me, and the grunt-whistle and head-up/tail-up, and so were in the midst of launching their own careers in on (Lorenz 1941). It seemed natural to regard these animal behavior. displays as instinctive or innate, and the concept of For young and old alike, Lehrman’s paper was innateness became central to his view of behavior. influential not only because of its cogent criticisms Ethologists then began describing how young of ethology, but also because of his eloquence, and animals of diverse species, raised under similar con- the tone in which it was written, which was ex- ditions, consistently developed distinctive behaviors tremely hostile. He almost ridiculed the concept that were sufficiently stable and stereotyped to yield of innateness, stressing the difficulty of excluding insights into taxonomy and phylogeny. Lorenz de- environmental influences on ontogeny, especially in veloped his notion of ‘fixed action patterns’, build- the study of behavior. By implication he called into ing on some of Heinroth’s ideas, characterizing units question the very idea that genetical approaches to of behavior that could be studied in similar terms to the study of behavioral development could be of anatomical and morphological features. value. Lorenz was furious and, although they be- This in turn was the view embraced by Tin- came reconciled later, I suspect that he never really bergen (1951) in his pivotal book on The Study of forgave Lehrman. At times the confrontation esca- Instinct. It appeared in the year I became a graduate lated and assumed an almost religious fervor. The student in Thorpe’s laboratory. Tinbergen’s com- aftermath of these angry exchanges could be felt mitment to the idea of innate behavior was clear and decades later, and I am convinced that the bitter- unequivocal. But over the next few years something ness of the controversy inhibited many in the next strange happened. Tinbergen made a radical change generation of behaviorists from even acknowledg- in his position on innateness.