Innate Learning Preferences: Signals for Communication PETER MARLER Departments of Psychology and Zoology Universio of California Davis, California
Research on the ways in which different species of birds learn to sing is used to illustrate the necessity of taking innate factors into account in studies of behavioral development. Experiments on two species of songbirds are described that reveal innate species differences in responsiveness to taperecorded songs. Conspecific songs are favored over those of other species. These patterns of innately varying responsiveness provide a basis for the development, not of stereotyped behavior, but of variable, individually learned behavior. The viewpoint is presented that mechanisms that differ innately from species to species, some with general functions, others specialized for particular ontogenetic assignments, provide the necessary substrates with which experience interacts.
As a result of controversy over the term “innate,” most students of animal behavior have eschewed its use altogether. As a consequence, ethological investigations of processes of behavioral epigenetics have been rendered largely impotent. The initiative has been left instead to geneticists and developmental biologists who take it for granted that the genome plays a major role in all aspects of behavioral development (Hirsch, 1967; Benzer, 1973; Gould, 1974; Hall, Greenspan, & Harris, 1982). One step towards a more enlightened viewpoint may derive from an appreciation of the insights into the underlying principles that derive from the appropriate application of the term “innate,” namely, to differences between organisms. It is perfectly valid to pose the question “To what extent are the differences observed between persons due to genotypic or to environmental causes?” (Dobzhansky, 1962, p. 44). “Evidence that a difference in behavior is to be ascribed to genetic differences must come ultimately from the rearing of animals, known to differ genetically, in similar environments” (Hinde, 1970, p. 431). This is the strategy adopted in a series of studies my colleagues and I have conducted on species differences in vocal learning in songbirds. In this account, the emphasis is placed on those particular differences that, because of the nature Reprint requests should be sent to Dr. Peter Marler, Dept. of Zoology, University of California, Davis, CA 95616. Received for publication 24 August 1988 Revised for publication 1 February 1989 Accepted at Wiley 13 July 1990 Developmental Psychobiology 557-568 (1990) 0 1990 by John Wiley & Sons, Inc.
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of the experimental design employed, can be attributed, not to contrasts in the environments in which they were raised, but to differences in their genetic constitution. They thus represent phenotypic differences that are ultimately attributable to genetic differences between the species (see Johnston, 1988, in litt.). Like the speech patterns of our own species, the songs of oscine birds are learned, passing from generation to generation by cultural transmission. Local dialects are common, and analogies have often been struck between dialects in birdsong and in speech (Mundinger, 1982; Baker & Cunningham, 1985). In terms of acoustic structure, birdsongs are among the most complex animal vocal signals known, rivaled only by the songs of certain cetaceans (Payne & McVay, 1971; Payne & Payne, 1985). Despite the obvious disparities in cognitive and semantic content, there are many parallels between the development of speech and birdsong if we consider them as culturally acquired motor patterns that provide the basis for a system of communication. As more is learned about the ontogeny of birdsong, it has become increasingly clear that each species of songbird has its own distinctive way of approaching the task of learning to sing (Marler, 1984:).Species differences can be discerned in the development of many aspects of the complex sensory and motor processing that is involved. The influence of innate species differences is so pervasive that a comprehensive understanding of the underlying mechanisms would be inconceivable without taking these differences into account (Marler & Sherman, 1985). This article concentrates on preferences for learning some songs rather than others as an illustration of one role that innate species differences may play in the vocal learning process.
Songbirds Have the Capacity to Acquire and Reproduce a Wide Range of Sounds The occurrence of song learning has been established with varying degrees of confidence in about 300 species of songbirds (Kroodsma, 1982),and it seems likely that patterns of male singing behavior are transmitted as learned cultural traditions in all 4000 or so species of songbirds. There are many illustrations of birds that were raised by aviculturalists out of earshot of songs of their own species but in the company of others, and that have acquired and reproduced alien songs that their species has never been heard to utter in nature. This is true not only of natural mimics such as starlings and mockingbirds but also of birds that rarely mimic species other than their own in the wild. It has been estimated that less than 1 in 10 species of songbird commonly mimics species other than its own in nature, yet the ability to render heterospecific songs with precision is evidently present. Even species that hew faithfully to the imitation of conspecific song in nature are occasionally recorded by observant ornithologists as reproducing the songs of another species (Eberhardt & Baptista, 1977; Baptista & Morton, 1981). A resourceful experimenter can greatly increase the probability of heterospecific imitation by caging young males in close proximity to singers of another species (Baptista & Petrinovich, 1984, 1986). What, then, accounts for the fact that songbirds in the wild almost always sing only the song of their own species? It is evident that the vocal apparatus of songbirds can produce a wider range of sounds than is typically observed under
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natural conditions, as when one species is taught to produce sounds of another that it does not normally imitate (Baptista & Petrinovich, 1986). By raising young male songbirds in the laboratory and giving them a choice of what to learn, it is possible to determine whether there are innate species differences in song learning preferences (Marler & Peters, 1988b, in press).
A Comparative Approach to the Innateness Problem: Learning Preferences in Sparrows A researcher who attempts a comprehensive analysis of learning preferences in a single species is faced with many difficulties, both practical and logical. The array of possible stimuli to test is potentially infinite. What guidelines should be employed in choosing which among many possible stimulus dimensions to subject to experimental variation? We have taken a comparative approach to this problem. Bird species have been selected that (a) live together in nature, within earshot of one another, so that they are required to make choices naturally and have done so in the course of their phylogenetic history; (b) are close relatives , sufficiently similar in general morphology and way of life that there is a good prospect of pinpointing differences in anatomy or physiology that might be responsible for behavioral variation; and (c) have songs that differ consistently in certain respects. Individuals of the two species are raised in identical environments so that they tell us if they are innately predisposed to respond differently to those environments. Song and swamp sparrows (Melospiza melodia and M . georgiana) are so close genetically that electrophoretic analyses of blood serum proteins yield very similar results (Zink, 1982). Natural hybrids occasionally survive. Their songs are both about 2.5 sec in duration, but the similarity ends there. Swamp sparrow song is a sequence of identical multinote syllables, delivered at a regular tempo (Fig. 1). In striking contrast with this simple one-phrased syntax (the term syntax refers here to temporal organization), song sparrow songs always comprise several distinct phrases of two distinct types, termed “trills” and “note complexes.” These syntactical complexities are lacking in swamp sparrow song. The two species differ in song tempo, which tends to be stable throughout a swamp sparrow song but varies within and between phrases in song sparrow song. The two species differ also in the size of individual song repertoires. Swamp sparrows average 3 song types per male, characterized by their distinctive syllabic structure. Individual male song sparrows have repertoires of 10 or 12 song types, and even larger ones in the western part of the species range. Song and swamp sparrows also differ in song phonology (the acoustic morphology of constituent notes). For example, all known swamp sparrow songs are constructed out of a relatively simple set of phonological units or notes used universally by all species members, with the arrangement of note types into syllables varying from one population to another (Marler & Pickert, 1984; Clark, Marler, & Beeman, 1987). In our usage, “syllables” are note clusters that are successively repeated in identical fashion. Geographical ‘‘dialects” can be characterized by the local rule for constructing syllables from notes, and Balaban (1988) has demonstrated that male and female swamp sparrows acquire responsiveness to local variations in the rules for syllabic syntax. Similarly, song sparrow song
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has a distinctive phonology, although the rules for organizing phonological units into phrases have not yet been fully analyzed. Thus, a sparrow that displays auditory preferences for learning certain songs, perhaps favoring songs of its own species over others, if the field evidence is any guide, has available numerous phonological and syntactical cues upon which a preference could be based.
Are There Learning Preferences or Are All Songs Equivalent as Learning Stimuli? We can visualize numerous ways in which the process of song acquisition might be biased to favor some songs over others. The visual appearance of a tutor might have an influence. Visual displays given as an accompaniment to singing could bias the process of song acquisition. There could be preferences in favor of songs emanating from tutors providing food or grooming opportunities or bearing a particular social relationship to the pupil, as would, for example, the dominant male in the local community or the bird’s father (Pepperberg, 1985; Baptista & Petrinovich, 1986; Clayton, 1988; King & West, 1988, this issue). The simplest case, most readily analyzable, is one in which a preference is exerted on the basis of acoustic cues alone. Unlike some songbirds, song and swamp sparrows will readily learn reliably from tape-recordings in the absence of any other social stimuli. How do male sparrows behave when given a choice of learning tape-recorded songs, some of which are from their own species and some from another species? In a typical experiment, tape-recordings are played daily to young male sparrows that, for convenience and ease of rearing, have been taken as nestlings in the wild at about 3 to 8 days after hatching, raised by hand in the laboratory, and kept in individual isolation. Experience with tape-recorded song is then provided during the sensitive period for song acquisition, which in these sparrows peaks between about 20 and 60 days of age (Marler & Peters, 1987, 1988a). To achieve a balanced design, two experiments are conducted in tandem, one with swamp sparrows as subjects and the other with song sparrows. Identical sets of tape-recordings are used in both cases, incorporating both song and swamp sparrow songs. Thus the stimulus subset that is heterospecific for one group of subjects is conspecific for the other. A typical result for such an experiment is shown in Figure 2. Singing behavior of all subjects is recorded on a weekly basis for the first year of life, until the birds are sexually mature, and analyzed by sound spectrograph for imitations. The outcome of such an experiment is clear. There is an overwhelming preference in favor of acquiring and reproducing songs of the bird’s own species. The experiment controls for the possibility that songs of one species might be inherently easier for any bird to learn than those of the other, because the very same songs preferred by one species are held in disfavor by the other. The result of such an experiment is rendered potentially ambiguous, however, by possible effects of experience of conspecific song in nature prior to bringing the nestlings into the labnrdtory. Although there is ample evidence to demonstrate that, in altricial species such as these, song experience as nestlings has no effect on song production later in life (Marler & Peters, 1980), such early experience
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might exert an influence on learning preferences. To explore this possibility a parallel series of experiments was conducted with males raised in isolation from even earlier stages of development. Eggs were taken from wild nests early in incubation, fostered under canaries in the laboratory, and again given the opportunity to learn tape-recorded songs of both species during the sensitive period for song acquisition. Analysis of songs produced later in life after the birds were maintained in individual isolation throughout the experiment, again revealed a strong bias in favor of conspecific song in both species (Marler & Peters, 1977; in press). We conclude that the species difference in learning preference is innate. Swamp and song sparrows differ in the degree to which a conspecific preference is manifest when tape-recorded song is used as the source of stimulation. The preference is more extreme in swamp sparrows than in song sparrows, which do imitate some swamp sparrow song. The preference was shown both in subjects reared as nestlings and in those reared from the egg (Fig. 2). There is evidently some discrepancy between the experimental test situation and that which occurs in nature. In the wild, song sparrows do not imitate swamp sparrows, despite the fact that they often live within earshot. Presumably some aspect of natural experience that is lacking from the highly simplified tape-recorded song paradigm is responsible for this disparity. Social factors of other kinds, involving perhaps specific visual responsiveness or social exchanges of an interactive nature, may also have potential effects on learning preferences. These factors may have more of an influence upon song sparrows than on swamp sparrows. In
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swamp sparrows, tape-recording and live tutor training paradigms have yielded very similar results (Marler & Peters, 1987), but a direct comparison has yet to be made in song sparrows. Using a quite different approach, employing cardiac responses as an index of responsiveness of juvenile song and swamp sparrows to song stimulation, Dooling and Searcy (1980) also found responsiveness of swamp sparrows to tape-recorded conspecific song to be more selective than that of song sparrows.
What Are the Acoustic Cues for Learning Preferences? By use of computer-synthesized songs in which some structural features have been systematically modified while leaving others unchanged, it has been shown that young male song and swamp sparrows respond to different aspects of song when they learn selectively (Marler & Peters, 1988b; 1989). Young swamp sparrows focus primarily on structure at the level of notes and syllables. When choosing songs for acquisition, male swamp sparrows are largely uninfluenced by the overall syntax of the song which, it will be recalled, is comparatively simple in this species. Exposure to multipartite songs does, however, result in the production of more two-phrased songs, even though one-phrased songs still predominate (Marler & Peters, 1980). Evidently male swamp sparrows are not completely unresponsive to song syntax. By contrast, song sparrows, with more complex songs, are responsive both to song phonology and to syntax in selective learning. There is some tradeoff between these two sets of features. A young male song sparrow may accept suboptimal phonological elements if they are presented within the framework of acceptable conspecific song syntax, and vice versa. The structural unit known as the note complex appears to play a special role in the responsiveness of song sparrows to song syntax (Fig. 3). The conclusion drawn from these studies is that there are innate learning preferences in song and swamp sparrows and innate differences in the stimulus cues on which the preferences are based. The relative emphasis on different song features differs between the two species, overall song syntax playing a weak role in learning preferences in swamp sparrows and a strong role in song sparrows (Marler & Peters, 1988b, 1989).
The Relationship Between Innateness and Learning It is not uncommon to hear the view expressed that learned and innate influences on behavioral development are in some sense antithetical. According to this position, behavior is one or the other, but is rarely, if ever, both. Innate behavior is displayed by “lower” animals, but our own species, apart from a few very basic drives, displays innate behavior rarely. Instead, we are supposed to be the manifestation of what can be achieved through the emancipation from innate controls (Gould & Marler, 1987). The antithesis implied by this viewpoint is patently false. Even the most extreme case of purely arbitrary, culturally transmitted behavior must in some sense be the result of innate mechanisms at work. The funtions of these innate mechanisms may be generalized, as when they are concerned with basic aspects
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of perception, or they may be highly specialized, as when they are involved in the memorization of stimuli to a particular end such as song learning or the development of speech. Without them, even the most creative aspects of development could not occur. Bird species differ strikingly in how long learned songs are stored before rehearsal begins and in the extent to which they remain faithful to learned models or modify them by processes of rearrangement, improvisation, and invention (Marler, 1984). Thus the question to be addressed is not “do innate mechanisms to learn exist?” but rather, “what is the nature of innate mechanisms for learning, by what mechanisms do they operate, and what provisions do they make for interaction between organisms and their environments?” In other words, what are the ways in which innate mechanisms impinge on the pervasive plasticity that behavior displays in the course of its development? Concepts from classical ethology such as innate releasers and innate release mechanisms are relevant here, with some shifts of emphasis (Lorenz, 1950;Tinbergen, 1951). These used to be thought of as rendering organisms virtually automatically responsive to certain stimulus contingencies that have assumed peculiar significance in the phylogenetic history of the species. In recent years, however, it has become clear that many such mechanisms have richer and more interesting functions than simply to serve as design features for animals as automata (Marler,
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1977; Marler, Dooling, & Zoloth, 1980). They also serve to facilitate and guide learning processes as one component in what can appropriately be viewed as innate mechanisms for learning. The intent of this article is to show that even with behavior that is as obviously learned as birdsong, innate mechanisms play a fundamental role in the learning process. This position follows naturally once it is appreciated that innate mechanisms are by no means immutable and lacking in ontogenetic plasticity but in fact provide those physiological substrates which are modifiable as a result of experience, It can be shown that even the most creative aspects of song development, such as vocal improvisation, are in some sense imbued with influences that differ innately from species to species (Marler, 1984). What are the consequences of regarding innate mechanisms as fundamental to the development of language and all other forms of communicative behavior, and indeed of all behavior? One advantage of this viewpoint is to remind us that, in studying such phenomena, we are dealing with the products of physiological mechanisms adapted to particular ends that vary from species to species. Thus in the conduct of observations and in the design and execution of experiments, we must be constantly alert for special predispositions brought to particular learning tasks, with the possibility that some specializations may be species specific. In the development of behaviors as specialized as human language or the complex use of the human face in recognition and social interaction, it would be surprising if innate mechanisms were not pervasively involved (Liberman & Mattingly , 1989; Locke, this issue). Some will have a wide phylogenetic distribution and others will be restricted to the human species, specifically adapted to the facilitation and guidance of the ontogeny of particular behaviors. Song learning preferences in birds serve as a simple version of the more complex case that confronts us in our own species. The invocation of innate influences in no way implies a commitment to completely stereotyped, inflexible patterns of development. Birds are innately responsive to certain features of conspecific song, but these abilities are used, not to generate stereotyped and immutable behavior in adulthood, but rather to guide the direction of processes of learning. The involvement of processes of song acquisition that differ innately from species to species does, however, impose certain probabilistic trajectories on patterns of behavioral development such that the mature song of two species will differ in predictable ways. In the normal course of species-typical development, there is little likelihood of young birds being deprived of the opportunity to favor songs of conspecifics over those of other species, even though they possess the competence to learn and reproduce a much wider range of sounds. Acknowledgment of the crucial role of learning mechanisms that vary innately from species to species results in potential benefits for the design of research strategies. Properly conducted, behavioral observations and experiments on the interaction between organisms and their environments in the course of ontogeny prepare the way in a direct manner for physiological investigation of the nature of the underlying mechanisms. From the viewpoint of psychological theory, an emphasis on species differences in learning predispositions may help to restrain overenthusiasm for general theories of learning, which seem inevitably to lead us to neglect of the critical developmental features of learned behaviors with specialized functions, such as language. Far from diminishing the importance of measuring
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and theorizing about the environments to which young organisms are exposed and from which they learn, the viewpoint adopted here places even more of an onus upon the observer/experimenter to exploit every biological insight available in the choice of which of the myriad of potential variables should be subjected to study and experiment. An arbitrary choice is likely to be at best of limited value, and at worst positively harmful, by leading to emphasis on experiential variables that, far from harmonizing with natural predispositions, are at odds with them. From the viewpoint of basic research, perhaps the most obvious and compelling reason for embracing the all-important role of innate species differences in the development of behavior, including those involved in language and communication, is that a full understanding of the underlying mechanisms is otherwise unattainable. Experience is an interactive process, and no organism is a passive victim of the environments it encounters in the course of development. Both innate factors and acquired information have a bearing on the development of any behavioral trait and how it is influenced by environmental stimulation (Lorenz, 19651, but the message of modern developmental biology is that, of all the components in the interactive equation, innate factors are the most basic. They set the stage for the emergence of all behavioral plasticity and establish the rules for interaction with the environment. Practical considerations may lead some experimenters to focus exclusively on the environmental components in the ontogenetic equation, but it is easy to be led astray. The great mistake of behaviorism was to deify this operational emphasis on the environment into the major principle underlying behavioral development. The difficulties, both practical and logical, confronting the researcher who seeks to understand the innate mechanisms underlying behavioral development must not be underestimated. Direct genetic manipulation provides the ideal approach. Meanwhile, appropriate application of comparative techniques bypasses at least some of the difficulties. One fruitful strategy is to make comparisons between species that behave differently and yet have sufficient in common in terms of brain structure that there is a resonable prospect of determining what mechanisms underlie the differences in their ontogeny . Apart from the special cases provided by genetic abnormalities and identicaltwin studies, studies of human behavior usually lack the powerful leverage provided by a strong comparative dimension. If by some quirk of history Neanderthals had survived, I suspect that our perspectives on the biological substrates of human behavioral development would be radically different. Lacking this comparative dimension, students of human behavior must turn to other disciplines to appreciate the full impact of the innateness argument. Nowhere is the full impact of the revolution in molecular genetics more evident than in developmental biology. Genes, once semimystical abstract entities, are now as amenable to experimentation as an organism’s environment. Eloquent arguments to the contrary notwithstanding (e.g., Oyama, 1985; Johnston, 1988), study of the impact of genes on behavioral development is both logically feasible and operationally tractable. It is increasingly clear that the links between genes and behavior can be surprisingly direct, and it is no longer inconceivable that genetic research may throw new light on the developmental basis of human behaviors. It behooves those of us who are students of behavioral development in both animals and humans to watch these developments closely and to follow their
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theoretical implications if we want to keep pace with the revelations of modern biology.
Note Research was conducted in collaboration with Susan Peters and supported in part by BRSG SO7 RR07065, awarded by the Biomedical Research Support Grant Program, Division of Research Resources, National Institutes of Health, and by Grant No. MH 14651. Esther Arruza prepared the figures and typed the manuscript. I thank Judith and Cathy Marler and Eileen McCue for rearing the birds. I am indebted to Susan Peters, Stephen Nowicki, Cathy Dent, Timothy Johnston, Meredith West, and Patricia Zukow for discussion and valuable criticism of the manuscript and to the New York Botanical Garden Institute of Ecosystem Studies at the Mary Flagler Cary Arboretum for access to study areas. This is a condensed version of a paper to be published in a book honoring Dr. Robert A. Hinde.
References Baker, M. C., & Cunningham, M. A. (1985). The biology of birdsong dialects. Behavioral and Brain Sciences, 8, 85-133. Balaban, E. (1988). Cultural and genetic variation in swamp sparrows (Melospiza georgiana): 11. Behavioral salience of geographic song variants. Behaviour, 105, 292-322. Baptista, L. F., & Morton, M. L. (1981). Interspecific song acquisition by a white-crowned sparrow. Auk, 98, 383-385. Baptista, L. F., & Petrinovich, L. (1984). Social interaction, sensitive phases and the song template hypothesis in the white-crowned sparrow. Animal Behaviour, 32, 172-181. Baptista, L. F., & Petrinovich, L. (1986). Song development in the white-crowned sparrow: Social factors and sex differences. Animal Behaviour, 34, 1359-1371. Benzer, S. (1973). Genetic dissection of behavior. Scientz3c American, 229, 24-37. Clark, C. W., Marler, P., & Beeman, K. (1987). Quantitative analysis of animal vocal phonology: An application to swamp sparrow song. Ethology, 76, 101-115. Clayton, N. S. (1988). Song tutor choice in zebra finches and Bengalese finches: The relative importance of visual and vocal cues. Behaviour, 104, 281-299. Dobzhansky, T. (1962). Mankind evolving. New Haven: Yale University Press. Dooling, R. J., & Searcy, M. H. (1980). Early perceptual selectivity in the swamp sparrow. Developmental Psychobiology, 13, 499-506. Eberhardt, C., & Baptista, L. F. (1977). Intraspecific and interspecific song mimesis in California song sparrows. Bird Banding, 48, 193-205. Gould, J. L. (1974). Genetics and molecular ethology. Zeitschrift f i r Tierpsychologie, 36, 267-292. Gould, J. L., & Marler, P. (1987). Learning by instinct. Scient8c American, 256, 74-85. Hall, J. C., Greenspan, R. J., & Harris, W. A. (Eds.). (1982). Genetic neurobiology. Cambridge: MIT Press. Hinde, R. A. (1970). Animal behaviour: A synthesis of ethology and comparative psychology (2nd ed.). New York: McGraw-Hill. Hirsch, J. (Ed.). (1967). Behavior-genetic analysis. New York: McGraw-Hill. Johnston, T. D. (1988). Developmental explanation and the ontogeny of birdsong: Nature/nurture redux. Behavioral and Brain Sciences, 1 1 , 631-675. King, A. P., & West, J. J. (1988). Searching for the functional origins of song in eastern brown-headed cowbirds, Molothrus ater ater. Animal Behaviour, 36, 1575-1588. King, A. P., & West, J. J. (1990). Communicating about communicating: When innate is not enough. Developmental Psychobiology, this issue. Kroodsma, D. (1982). Learning and the ontogeny of sound signals in birds. In D. E. Kroodsma & E. H. Miller (Eds.), Acoustic Communication in birds (Vol. 2, pp. 1-23. New York: Academic Press. Liberman, A. M., & Mattingly, I. G. (1989). A specialization for speech perception. Science, 243, 489-494.
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Locke, M. (1990). Structure and stimulation in the ontogeny of spoken language. Developmental Psychobiology, this issue. Lorenz, K. Z . (1950). The comparative method in studying innate behavior patterns. Symposia of the Society of Experimental Biology, 4 , 221-268. Lorenz, K. S . (1965). Evolution and modification of behavior. Chicago: Chicago University Press. Marler, P. (1977). Development and learning of recognition systems. In T. H. Bullock (Ed.), Recognition of complex acoustic signals (pp. 77-96). Berlin: Dahlem Konferenzen. Marler, P. (1984). Song learning: Innate species differences in the learning process. In P. Marler and H. S. Terrace (Eds.), The biology qf learning (pp. 289-309). Berlin: Springer-Verlag. Marler, P., Dooling, R., & Zoloth, S. (1980). Comparative perspectives on ethology and perceptual development. In M. Bornstein (Ed.), The Comparative method in psychology: Ethological, developmental and cross-cultural viewpoints (pp. 189-230). Hillsdale, NJ: Erlbaum. Marler, P., & Peters, S. (1977). Selective vocal learning in a sparrow. Science, 198, 519-521. Marler, P., & Peters, S . (1980). Birdsong and speech: Evidence for special processing. In P. Eimas and J . Miller (Eds.), perspectives on the study of speech (pp. 75-112). Hillsdale, NJ: Erlbaum. Marler, P., & Peters, S. (1987). A sensitive period for song acquisition in the song sparrow, Melospiza rnelodia: A case of age-limited learning. Ethology, 76, 89-100. Marler, P.. & Peters, S. (1988a). Sensitive periods for song acquisition from tape recordings and live tutors in the swamp sparrow, Melospiza georgiana. Ethology, 77, 76-84. Marler, P., & Peters, S. (1988b). The role of song phonology and syntax in vocal learning preferences in the song sparrow, Melospiza melodia. Ethology, 77, 125-149. Marler, P., & Peters, S. (1989). Species differences in auditory responsiveness in early vocal learning. In S. Hulse & R. Dooling (Eds.), The comparative psychology of complex acoustic perception. Hillsdale, NJ: Erlbaum. Marler, P., & Pickert, R. (1984). Species-universal microstructure in the learned song of the swamp sparrow (Melospiza georgiana). Animal Behaviour, 32, 673-689. Marler, P., & Sherman, V. (1985). Innate differences in singing behaviour of sparrows reared in isolation from adult conspecific song. Animal Behaviour, 33, 57-71. Mundinger, P. (1982). Microgeographic and macrogeographic variation in the acquired vocalizations of birds. In D. Kroodsma & E. Miller (Eds.), Acoustic communication in birds (Vol. 2, pp. 147-208). New York: Academic Press. Oyama, S. (1985). The ontogeny of information: Developmental systems and evolution. Cambridge: Cambridge University Press. Payne, R . S . , & McVay, S. (1971). Songs of humpback whales. Science, 173, 587-597. Payne, K . , & Payne, R. (1985). Large scale changes over 19 years in songs of humpback whales in Bermuda. Zeitschrift fur Tierpsychologie, 68, 89-1 14. Pepperberg. I. M. (1985). Social modelling theory: A possible framework for understanding avian vocal learning. Auk, 102, 854-864. Tinbergen, N. (1951). The study of instinct. Oxford: Clarendon. Zink, R. M. (1982). Patterns of genic and morphologic variation among sparrows in the genera Zonotrichiu, Melospiza, Junco, and Passerella. Auk, 99, 632-649.
Research on the ways in which different species of birds learn to sing is used to illustrate the necessity of taking innate factors into account in studies of behavioral development. Experiments on two species of songbirds are described that reveal innate species differences in responsiveness to taperecorded songs. Conspecific songs are favored over those of other species. These patterns of innately varying responsiveness provide a basis for the development, not of stereotyped behavior, but of variable, individually learned behavior. The viewpoint is presented that mechanisms that differ innately from species to species, some with general functions, others specialized for particular ontogenetic assignments, provide the necessary substrates with which experience interacts.
As a result of controversy over the term “innate,” most students of animal behavior have eschewed its use altogether. As a consequence, ethological investigations of processes of behavioral epigenetics have been rendered largely impotent. The initiative has been left instead to geneticists and developmental biologists who take it for granted that the genome plays a major role in all aspects of behavioral development (Hirsch, 1967; Benzer, 1973; Gould, 1974; Hall, Greenspan, & Harris, 1982). One step towards a more enlightened viewpoint may derive from an appreciation of the insights into the underlying principles that derive from the appropriate application of the term “innate,” namely, to differences between organisms. It is perfectly valid to pose the question “To what extent are the differences observed between persons due to genotypic or to environmental causes?” (Dobzhansky, 1962, p. 44). “Evidence that a difference in behavior is to be ascribed to genetic differences must come ultimately from the rearing of animals, known to differ genetically, in similar environments” (Hinde, 1970, p. 431). This is the strategy adopted in a series of studies my colleagues and I have conducted on species differences in vocal learning in songbirds. In this account, the emphasis is placed on those particular differences that, because of the nature Reprint requests should be sent to Dr. Peter Marler, Dept. of Zoology, University of California, Davis, CA 95616. Received for publication 24 August 1988 Revised for publication 1 February 1989 Accepted at Wiley 13 July 1990 Developmental Psychobiology 557-568 (1990) 0 1990 by John Wiley & Sons, Inc.
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of the experimental design employed, can be attributed, not to contrasts in the environments in which they were raised, but to differences in their genetic constitution. They thus represent phenotypic differences that are ultimately attributable to genetic differences between the species (see Johnston, 1988, in litt.). Like the speech patterns of our own species, the songs of oscine birds are learned, passing from generation to generation by cultural transmission. Local dialects are common, and analogies have often been struck between dialects in birdsong and in speech (Mundinger, 1982; Baker & Cunningham, 1985). In terms of acoustic structure, birdsongs are among the most complex animal vocal signals known, rivaled only by the songs of certain cetaceans (Payne & McVay, 1971; Payne & Payne, 1985). Despite the obvious disparities in cognitive and semantic content, there are many parallels between the development of speech and birdsong if we consider them as culturally acquired motor patterns that provide the basis for a system of communication. As more is learned about the ontogeny of birdsong, it has become increasingly clear that each species of songbird has its own distinctive way of approaching the task of learning to sing (Marler, 1984:).Species differences can be discerned in the development of many aspects of the complex sensory and motor processing that is involved. The influence of innate species differences is so pervasive that a comprehensive understanding of the underlying mechanisms would be inconceivable without taking these differences into account (Marler & Sherman, 1985). This article concentrates on preferences for learning some songs rather than others as an illustration of one role that innate species differences may play in the vocal learning process.
Songbirds Have the Capacity to Acquire and Reproduce a Wide Range of Sounds The occurrence of song learning has been established with varying degrees of confidence in about 300 species of songbirds (Kroodsma, 1982),and it seems likely that patterns of male singing behavior are transmitted as learned cultural traditions in all 4000 or so species of songbirds. There are many illustrations of birds that were raised by aviculturalists out of earshot of songs of their own species but in the company of others, and that have acquired and reproduced alien songs that their species has never been heard to utter in nature. This is true not only of natural mimics such as starlings and mockingbirds but also of birds that rarely mimic species other than their own in the wild. It has been estimated that less than 1 in 10 species of songbird commonly mimics species other than its own in nature, yet the ability to render heterospecific songs with precision is evidently present. Even species that hew faithfully to the imitation of conspecific song in nature are occasionally recorded by observant ornithologists as reproducing the songs of another species (Eberhardt & Baptista, 1977; Baptista & Morton, 1981). A resourceful experimenter can greatly increase the probability of heterospecific imitation by caging young males in close proximity to singers of another species (Baptista & Petrinovich, 1984, 1986). What, then, accounts for the fact that songbirds in the wild almost always sing only the song of their own species? It is evident that the vocal apparatus of songbirds can produce a wider range of sounds than is typically observed under
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natural conditions, as when one species is taught to produce sounds of another that it does not normally imitate (Baptista & Petrinovich, 1986). By raising young male songbirds in the laboratory and giving them a choice of what to learn, it is possible to determine whether there are innate species differences in song learning preferences (Marler & Peters, 1988b, in press).
A Comparative Approach to the Innateness Problem: Learning Preferences in Sparrows A researcher who attempts a comprehensive analysis of learning preferences in a single species is faced with many difficulties, both practical and logical. The array of possible stimuli to test is potentially infinite. What guidelines should be employed in choosing which among many possible stimulus dimensions to subject to experimental variation? We have taken a comparative approach to this problem. Bird species have been selected that (a) live together in nature, within earshot of one another, so that they are required to make choices naturally and have done so in the course of their phylogenetic history; (b) are close relatives , sufficiently similar in general morphology and way of life that there is a good prospect of pinpointing differences in anatomy or physiology that might be responsible for behavioral variation; and (c) have songs that differ consistently in certain respects. Individuals of the two species are raised in identical environments so that they tell us if they are innately predisposed to respond differently to those environments. Song and swamp sparrows (Melospiza melodia and M . georgiana) are so close genetically that electrophoretic analyses of blood serum proteins yield very similar results (Zink, 1982). Natural hybrids occasionally survive. Their songs are both about 2.5 sec in duration, but the similarity ends there. Swamp sparrow song is a sequence of identical multinote syllables, delivered at a regular tempo (Fig. 1). In striking contrast with this simple one-phrased syntax (the term syntax refers here to temporal organization), song sparrow songs always comprise several distinct phrases of two distinct types, termed “trills” and “note complexes.” These syntactical complexities are lacking in swamp sparrow song. The two species differ in song tempo, which tends to be stable throughout a swamp sparrow song but varies within and between phrases in song sparrow song. The two species differ also in the size of individual song repertoires. Swamp sparrows average 3 song types per male, characterized by their distinctive syllabic structure. Individual male song sparrows have repertoires of 10 or 12 song types, and even larger ones in the western part of the species range. Song and swamp sparrows also differ in song phonology (the acoustic morphology of constituent notes). For example, all known swamp sparrow songs are constructed out of a relatively simple set of phonological units or notes used universally by all species members, with the arrangement of note types into syllables varying from one population to another (Marler & Pickert, 1984; Clark, Marler, & Beeman, 1987). In our usage, “syllables” are note clusters that are successively repeated in identical fashion. Geographical ‘‘dialects” can be characterized by the local rule for constructing syllables from notes, and Balaban (1988) has demonstrated that male and female swamp sparrows acquire responsiveness to local variations in the rules for syllabic syntax. Similarly, song sparrow song
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has a distinctive phonology, although the rules for organizing phonological units into phrases have not yet been fully analyzed. Thus, a sparrow that displays auditory preferences for learning certain songs, perhaps favoring songs of its own species over others, if the field evidence is any guide, has available numerous phonological and syntactical cues upon which a preference could be based.
Are There Learning Preferences or Are All Songs Equivalent as Learning Stimuli? We can visualize numerous ways in which the process of song acquisition might be biased to favor some songs over others. The visual appearance of a tutor might have an influence. Visual displays given as an accompaniment to singing could bias the process of song acquisition. There could be preferences in favor of songs emanating from tutors providing food or grooming opportunities or bearing a particular social relationship to the pupil, as would, for example, the dominant male in the local community or the bird’s father (Pepperberg, 1985; Baptista & Petrinovich, 1986; Clayton, 1988; King & West, 1988, this issue). The simplest case, most readily analyzable, is one in which a preference is exerted on the basis of acoustic cues alone. Unlike some songbirds, song and swamp sparrows will readily learn reliably from tape-recordings in the absence of any other social stimuli. How do male sparrows behave when given a choice of learning tape-recorded songs, some of which are from their own species and some from another species? In a typical experiment, tape-recordings are played daily to young male sparrows that, for convenience and ease of rearing, have been taken as nestlings in the wild at about 3 to 8 days after hatching, raised by hand in the laboratory, and kept in individual isolation. Experience with tape-recorded song is then provided during the sensitive period for song acquisition, which in these sparrows peaks between about 20 and 60 days of age (Marler & Peters, 1987, 1988a). To achieve a balanced design, two experiments are conducted in tandem, one with swamp sparrows as subjects and the other with song sparrows. Identical sets of tape-recordings are used in both cases, incorporating both song and swamp sparrow songs. Thus the stimulus subset that is heterospecific for one group of subjects is conspecific for the other. A typical result for such an experiment is shown in Figure 2. Singing behavior of all subjects is recorded on a weekly basis for the first year of life, until the birds are sexually mature, and analyzed by sound spectrograph for imitations. The outcome of such an experiment is clear. There is an overwhelming preference in favor of acquiring and reproducing songs of the bird’s own species. The experiment controls for the possibility that songs of one species might be inherently easier for any bird to learn than those of the other, because the very same songs preferred by one species are held in disfavor by the other. The result of such an experiment is rendered potentially ambiguous, however, by possible effects of experience of conspecific song in nature prior to bringing the nestlings into the labnrdtory. Although there is ample evidence to demonstrate that, in altricial species such as these, song experience as nestlings has no effect on song production later in life (Marler & Peters, 1980), such early experience
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might exert an influence on learning preferences. To explore this possibility a parallel series of experiments was conducted with males raised in isolation from even earlier stages of development. Eggs were taken from wild nests early in incubation, fostered under canaries in the laboratory, and again given the opportunity to learn tape-recorded songs of both species during the sensitive period for song acquisition. Analysis of songs produced later in life after the birds were maintained in individual isolation throughout the experiment, again revealed a strong bias in favor of conspecific song in both species (Marler & Peters, 1977; in press). We conclude that the species difference in learning preference is innate. Swamp and song sparrows differ in the degree to which a conspecific preference is manifest when tape-recorded song is used as the source of stimulation. The preference is more extreme in swamp sparrows than in song sparrows, which do imitate some swamp sparrow song. The preference was shown both in subjects reared as nestlings and in those reared from the egg (Fig. 2). There is evidently some discrepancy between the experimental test situation and that which occurs in nature. In the wild, song sparrows do not imitate swamp sparrows, despite the fact that they often live within earshot. Presumably some aspect of natural experience that is lacking from the highly simplified tape-recorded song paradigm is responsible for this disparity. Social factors of other kinds, involving perhaps specific visual responsiveness or social exchanges of an interactive nature, may also have potential effects on learning preferences. These factors may have more of an influence upon song sparrows than on swamp sparrows. In
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swamp sparrows, tape-recording and live tutor training paradigms have yielded very similar results (Marler & Peters, 1987), but a direct comparison has yet to be made in song sparrows. Using a quite different approach, employing cardiac responses as an index of responsiveness of juvenile song and swamp sparrows to song stimulation, Dooling and Searcy (1980) also found responsiveness of swamp sparrows to tape-recorded conspecific song to be more selective than that of song sparrows.
What Are the Acoustic Cues for Learning Preferences? By use of computer-synthesized songs in which some structural features have been systematically modified while leaving others unchanged, it has been shown that young male song and swamp sparrows respond to different aspects of song when they learn selectively (Marler & Peters, 1988b; 1989). Young swamp sparrows focus primarily on structure at the level of notes and syllables. When choosing songs for acquisition, male swamp sparrows are largely uninfluenced by the overall syntax of the song which, it will be recalled, is comparatively simple in this species. Exposure to multipartite songs does, however, result in the production of more two-phrased songs, even though one-phrased songs still predominate (Marler & Peters, 1980). Evidently male swamp sparrows are not completely unresponsive to song syntax. By contrast, song sparrows, with more complex songs, are responsive both to song phonology and to syntax in selective learning. There is some tradeoff between these two sets of features. A young male song sparrow may accept suboptimal phonological elements if they are presented within the framework of acceptable conspecific song syntax, and vice versa. The structural unit known as the note complex appears to play a special role in the responsiveness of song sparrows to song syntax (Fig. 3). The conclusion drawn from these studies is that there are innate learning preferences in song and swamp sparrows and innate differences in the stimulus cues on which the preferences are based. The relative emphasis on different song features differs between the two species, overall song syntax playing a weak role in learning preferences in swamp sparrows and a strong role in song sparrows (Marler & Peters, 1988b, 1989).
The Relationship Between Innateness and Learning It is not uncommon to hear the view expressed that learned and innate influences on behavioral development are in some sense antithetical. According to this position, behavior is one or the other, but is rarely, if ever, both. Innate behavior is displayed by “lower” animals, but our own species, apart from a few very basic drives, displays innate behavior rarely. Instead, we are supposed to be the manifestation of what can be achieved through the emancipation from innate controls (Gould & Marler, 1987). The antithesis implied by this viewpoint is patently false. Even the most extreme case of purely arbitrary, culturally transmitted behavior must in some sense be the result of innate mechanisms at work. The funtions of these innate mechanisms may be generalized, as when they are concerned with basic aspects
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Fig. 3. Song learning preferences of young male song sparrows presented with tape recordings of normal songs (A) and synthetic song with one, two, or three segments (B, C, D). In every experiment subjects had a choice between conspecific and heterospecific (swamp sparrow) syllables. A illustrates the conspecific preference with normal song. B shows a significant preference based on phonology and syllable structure alone. C illustrates loss of the conspecific preference with two-phrased songs. D shows reinstatement of a conspecific syllable preference by addition of a note complex to C. The data are summarized from several experiments in Marler and Peters (1988b).
of perception, or they may be highly specialized, as when they are involved in the memorization of stimuli to a particular end such as song learning or the development of speech. Without them, even the most creative aspects of development could not occur. Bird species differ strikingly in how long learned songs are stored before rehearsal begins and in the extent to which they remain faithful to learned models or modify them by processes of rearrangement, improvisation, and invention (Marler, 1984). Thus the question to be addressed is not “do innate mechanisms to learn exist?” but rather, “what is the nature of innate mechanisms for learning, by what mechanisms do they operate, and what provisions do they make for interaction between organisms and their environments?” In other words, what are the ways in which innate mechanisms impinge on the pervasive plasticity that behavior displays in the course of its development? Concepts from classical ethology such as innate releasers and innate release mechanisms are relevant here, with some shifts of emphasis (Lorenz, 1950;Tinbergen, 1951). These used to be thought of as rendering organisms virtually automatically responsive to certain stimulus contingencies that have assumed peculiar significance in the phylogenetic history of the species. In recent years, however, it has become clear that many such mechanisms have richer and more interesting functions than simply to serve as design features for animals as automata (Marler,
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1977; Marler, Dooling, & Zoloth, 1980). They also serve to facilitate and guide learning processes as one component in what can appropriately be viewed as innate mechanisms for learning. The intent of this article is to show that even with behavior that is as obviously learned as birdsong, innate mechanisms play a fundamental role in the learning process. This position follows naturally once it is appreciated that innate mechanisms are by no means immutable and lacking in ontogenetic plasticity but in fact provide those physiological substrates which are modifiable as a result of experience, It can be shown that even the most creative aspects of song development, such as vocal improvisation, are in some sense imbued with influences that differ innately from species to species (Marler, 1984). What are the consequences of regarding innate mechanisms as fundamental to the development of language and all other forms of communicative behavior, and indeed of all behavior? One advantage of this viewpoint is to remind us that, in studying such phenomena, we are dealing with the products of physiological mechanisms adapted to particular ends that vary from species to species. Thus in the conduct of observations and in the design and execution of experiments, we must be constantly alert for special predispositions brought to particular learning tasks, with the possibility that some specializations may be species specific. In the development of behaviors as specialized as human language or the complex use of the human face in recognition and social interaction, it would be surprising if innate mechanisms were not pervasively involved (Liberman & Mattingly , 1989; Locke, this issue). Some will have a wide phylogenetic distribution and others will be restricted to the human species, specifically adapted to the facilitation and guidance of the ontogeny of particular behaviors. Song learning preferences in birds serve as a simple version of the more complex case that confronts us in our own species. The invocation of innate influences in no way implies a commitment to completely stereotyped, inflexible patterns of development. Birds are innately responsive to certain features of conspecific song, but these abilities are used, not to generate stereotyped and immutable behavior in adulthood, but rather to guide the direction of processes of learning. The involvement of processes of song acquisition that differ innately from species to species does, however, impose certain probabilistic trajectories on patterns of behavioral development such that the mature song of two species will differ in predictable ways. In the normal course of species-typical development, there is little likelihood of young birds being deprived of the opportunity to favor songs of conspecifics over those of other species, even though they possess the competence to learn and reproduce a much wider range of sounds. Acknowledgment of the crucial role of learning mechanisms that vary innately from species to species results in potential benefits for the design of research strategies. Properly conducted, behavioral observations and experiments on the interaction between organisms and their environments in the course of ontogeny prepare the way in a direct manner for physiological investigation of the nature of the underlying mechanisms. From the viewpoint of psychological theory, an emphasis on species differences in learning predispositions may help to restrain overenthusiasm for general theories of learning, which seem inevitably to lead us to neglect of the critical developmental features of learned behaviors with specialized functions, such as language. Far from diminishing the importance of measuring
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and theorizing about the environments to which young organisms are exposed and from which they learn, the viewpoint adopted here places even more of an onus upon the observer/experimenter to exploit every biological insight available in the choice of which of the myriad of potential variables should be subjected to study and experiment. An arbitrary choice is likely to be at best of limited value, and at worst positively harmful, by leading to emphasis on experiential variables that, far from harmonizing with natural predispositions, are at odds with them. From the viewpoint of basic research, perhaps the most obvious and compelling reason for embracing the all-important role of innate species differences in the development of behavior, including those involved in language and communication, is that a full understanding of the underlying mechanisms is otherwise unattainable. Experience is an interactive process, and no organism is a passive victim of the environments it encounters in the course of development. Both innate factors and acquired information have a bearing on the development of any behavioral trait and how it is influenced by environmental stimulation (Lorenz, 19651, but the message of modern developmental biology is that, of all the components in the interactive equation, innate factors are the most basic. They set the stage for the emergence of all behavioral plasticity and establish the rules for interaction with the environment. Practical considerations may lead some experimenters to focus exclusively on the environmental components in the ontogenetic equation, but it is easy to be led astray. The great mistake of behaviorism was to deify this operational emphasis on the environment into the major principle underlying behavioral development. The difficulties, both practical and logical, confronting the researcher who seeks to understand the innate mechanisms underlying behavioral development must not be underestimated. Direct genetic manipulation provides the ideal approach. Meanwhile, appropriate application of comparative techniques bypasses at least some of the difficulties. One fruitful strategy is to make comparisons between species that behave differently and yet have sufficient in common in terms of brain structure that there is a resonable prospect of determining what mechanisms underlie the differences in their ontogeny . Apart from the special cases provided by genetic abnormalities and identicaltwin studies, studies of human behavior usually lack the powerful leverage provided by a strong comparative dimension. If by some quirk of history Neanderthals had survived, I suspect that our perspectives on the biological substrates of human behavioral development would be radically different. Lacking this comparative dimension, students of human behavior must turn to other disciplines to appreciate the full impact of the innateness argument. Nowhere is the full impact of the revolution in molecular genetics more evident than in developmental biology. Genes, once semimystical abstract entities, are now as amenable to experimentation as an organism’s environment. Eloquent arguments to the contrary notwithstanding (e.g., Oyama, 1985; Johnston, 1988), study of the impact of genes on behavioral development is both logically feasible and operationally tractable. It is increasingly clear that the links between genes and behavior can be surprisingly direct, and it is no longer inconceivable that genetic research may throw new light on the developmental basis of human behaviors. It behooves those of us who are students of behavioral development in both animals and humans to watch these developments closely and to follow their
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theoretical implications if we want to keep pace with the revelations of modern biology.
Note Research was conducted in collaboration with Susan Peters and supported in part by BRSG SO7 RR07065, awarded by the Biomedical Research Support Grant Program, Division of Research Resources, National Institutes of Health, and by Grant No. MH 14651. Esther Arruza prepared the figures and typed the manuscript. I thank Judith and Cathy Marler and Eileen McCue for rearing the birds. I am indebted to Susan Peters, Stephen Nowicki, Cathy Dent, Timothy Johnston, Meredith West, and Patricia Zukow for discussion and valuable criticism of the manuscript and to the New York Botanical Garden Institute of Ecosystem Studies at the Mary Flagler Cary Arboretum for access to study areas. This is a condensed version of a paper to be published in a book honoring Dr. Robert A. Hinde.
References Baker, M. C., & Cunningham, M. A. (1985). The biology of birdsong dialects. Behavioral and Brain Sciences, 8, 85-133. Balaban, E. (1988). Cultural and genetic variation in swamp sparrows (Melospiza georgiana): 11. Behavioral salience of geographic song variants. Behaviour, 105, 292-322. Baptista, L. F., & Morton, M. L. (1981). Interspecific song acquisition by a white-crowned sparrow. Auk, 98, 383-385. Baptista, L. F., & Petrinovich, L. (1984). Social interaction, sensitive phases and the song template hypothesis in the white-crowned sparrow. Animal Behaviour, 32, 172-181. Baptista, L. F., & Petrinovich, L. (1986). Song development in the white-crowned sparrow: Social factors and sex differences. Animal Behaviour, 34, 1359-1371. Benzer, S. (1973). Genetic dissection of behavior. Scientz3c American, 229, 24-37. Clark, C. W., Marler, P., & Beeman, K. (1987). Quantitative analysis of animal vocal phonology: An application to swamp sparrow song. Ethology, 76, 101-115. Clayton, N. S. (1988). Song tutor choice in zebra finches and Bengalese finches: The relative importance of visual and vocal cues. Behaviour, 104, 281-299. Dobzhansky, T. (1962). Mankind evolving. New Haven: Yale University Press. Dooling, R. J., & Searcy, M. H. (1980). Early perceptual selectivity in the swamp sparrow. Developmental Psychobiology, 13, 499-506. Eberhardt, C., & Baptista, L. F. (1977). Intraspecific and interspecific song mimesis in California song sparrows. Bird Banding, 48, 193-205. Gould, J. L. (1974). Genetics and molecular ethology. Zeitschrift f i r Tierpsychologie, 36, 267-292. Gould, J. L., & Marler, P. (1987). Learning by instinct. Scient8c American, 256, 74-85. Hall, J. C., Greenspan, R. J., & Harris, W. A. (Eds.). (1982). Genetic neurobiology. Cambridge: MIT Press. Hinde, R. A. (1970). Animal behaviour: A synthesis of ethology and comparative psychology (2nd ed.). New York: McGraw-Hill. Hirsch, J. (Ed.). (1967). Behavior-genetic analysis. New York: McGraw-Hill. Johnston, T. D. (1988). Developmental explanation and the ontogeny of birdsong: Nature/nurture redux. Behavioral and Brain Sciences, 1 1 , 631-675. King, A. P., & West, J. J. (1988). Searching for the functional origins of song in eastern brown-headed cowbirds, Molothrus ater ater. Animal Behaviour, 36, 1575-1588. King, A. P., & West, J. J. (1990). Communicating about communicating: When innate is not enough. Developmental Psychobiology, this issue. Kroodsma, D. (1982). Learning and the ontogeny of sound signals in birds. In D. E. Kroodsma & E. H. Miller (Eds.), Acoustic Communication in birds (Vol. 2, pp. 1-23. New York: Academic Press. Liberman, A. M., & Mattingly, I. G. (1989). A specialization for speech perception. Science, 243, 489-494.
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