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Johan Bolhuis

Abstract

The four questions that Niko Tinbergen identified for behavioural biology — evolution, function, development and causation — are all important and should be studied in their own right. Recently, there has been a debate as to whether these four questions should be investigated separately or whether they should be integrated. Integration of the four questions has been attempted in novel research disciplines such as cognitive ecology, evolutionary psychology and neuroecology. Euan Macphail and I have criticised these integrative approaches, suggesting that they are fundamentally flawed as they confound function and mechanism. Investigating the function or evolutionary history of a behaviour or cognitive system is important and entirely legitimate. However, such investigations cannot provide us with answers to questions about the mechanisms underlying behaviour or cognition. At most, functional or evolutionary considerations can provide clues that may be useful for a causal analysis of the underlying mechanisms. However, these clues can be misleading and are often wrong, as is illustrated with examples from song learning and food storing in birds. After summarising the main issues in the neuroecology debate, I discuss some misunderstandings that were apparent in the responses to our critique, as well as some recent relevant data. Recent results do not support the neuroecological approach. Finally, I suggest that the way forward is a cautious and critical use of functional and evolutionary clues in the study of the mechanisms of behaviour.

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Jerry Hogan and Johan Bolhuis

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Niko Tinbergen (1963) put behavioural development on the map as one of the four main problems in behavioural biology. Developmental research at the time was still in the grip of the nature/nurture debate. In his discussion, Tinbergen advocated an interactionist approach to development, which has been the main point of view in developmental research since then. In this paper, we review research in a number of different areas, including imprinting, song learning, motivational systems, human language, and attachment. It has become clear that sensitive periods are important in all these areas, and that some aspects of development are generally irreversible; but these phenomena are not as rigid as was thought previously. Similarly, predispositions, or biases, play an important role in perceptual development, but here too there is much more flexibility than is sometimes suggested. Learning mechanisms underlying imprinting and song acquisition are very similar to those underlying other forms of associative learning. Cognitive concepts such as neural representations and behaviour systems are becoming more common in the analysis of developmental questions. Finally, there are numerous parallels between developmental processes in humans and other animals.

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Evolution, Function, Development and Causation

Tinbergen's Four Questions and Contemporary Behavioural Biology

Edited by Johan Bolhuis and Simon Verhulst

Ethologist and Nobel laureate Niko Tinbergen laid the foundations for the scientific study of animal behaviour when he formulated its four main problems: evolution, function, development and causation. Celebrating the fortieth anniversary of the publication of Tinbergen’s classic article ‘On aims and methods of ethology’, in this book an international cast of leading behavioural biologists reflect on the enduring significance of his groundbreaking proposals. Following a reprint of Tinbergen’s seminal paper on the famous ‘four why’s’, a contemporary perspective is presented on each of the four problems. In addition, two essays discuss the wider significance of recent trends in evolutionary psychology and neuroecology to integrate the four why’s. This wide ranging book, with a foreword by Aubrey Manning, will appeal to students and researchers in behavioural biology, experimental psychology and cognitive neuroscience.
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Hiroko Eda-Fujiwara and Johan Bolhuis

Abstract

The males of songbirds and parrots learn their songs from a tutor. Until recently it was thought that in songbirds, brain nuclei in the so-called 'song system' were involved in song learning, in addition to their role in song perception and production. Experiments involving measurement of the expression of immediate early genes (IEG) showed that exposure to song leads to activation of cells in brain regions outside the song system, notably the caudomedial neostriatum (NCM) and the caudomedial hyperstriatum ventrale (CMHV), suggesting that these regions are involved in auditory perception. In addition, neuronal activation in the NCM correlates with the number of song elements that a male has learned from its tutor, suggesting that NCM may be (part of) the neural substrate for stored tutor song. Songbird females do not usually sing, but nevertheless they can learn the characteristics of tutor song, and they can develop a perceptual preference for tutor song over novel song. When exposed to male song, female songbirds and parrots show increased IEG expression in NCM and CMHV that is related to song complexity. In addition, the IEG response in the NCM (and perhaps in the CMHV) of female songbirds may also be related to song learning.

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Johan J. Bolhuis and Hendrik S. Van Kampen

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Johan J. Bolhuis and Hendrik S. VAN KAMPEN

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Gabriel Horn, Johan J. Bolhuis and Neil G. Hampton

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Filial preferences in young domestic chicks, Gallus gallus domesticus, are influenced by at least two systems: one involved in learning about stimuli to which the animals are exposed, and the other a predisposition to approach stimuli resembling conspecifics. The predisposition is manifest in dark-reared chicks as an emerging preference for a rotating, stuffed jungle fowl over a rotating red box. In previous studies, 24 h-old visually naive chicks were placed in running wheels for 2 h. Throughout this time the chicks were in darkness. A significant preference for the stuffed fowl was found 24 h, but not 2 h later. In the present study it was shown that the predisposition becomes manifest at 10 h (Experiment la) and 5 h (Experiment 1 b) after either placement in running wheels, or after the chicks had been trained by exposure to a rotating red box. In Experiment 2 it was shown that placement in running wheels was not necessary for the predisposition to emerge. However, handling the birds was sufficient for the induction of a significant preference, expressed 5 h later. Exposure to a maternal call for 2 h (Experiment 3) was also sufficient to induce the development of the visual predisposition 24 h later. These results show that a visual predisposition to approach certain stimuli becomes manifest in dark-reared chicks between 2 and 5 h after the experience of handling, and that exposure to a maternal call is also sufficient to induce this predisposition.