Review
Tinbergen's four questions: an appreciation and an update

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Highlights

  • We show that, 50 years after first formulated, Tinbergen's four questions remain valid.

  • We update Tinbergen's four questions in the light of recent findings.

  • We stress how the questions may sometimes need to be considered together.

  • We point to questions additional to those of Tinbergen such as ‘How is the behaviour inherited?’, ‘What is the character?’, and ‘Of what is an animal seemingly aware?’.

This year is the 50th anniversary of Tinbergen's (1963) article ‘On aims and methods of ethology’, where he first outlined the four ‘major problems of biology’. The classification of the four problems, or questions, is one of Tinbergen's most enduring legacies, and it remains as valuable today as 50 years ago in highlighting the value of a comprehensive, multifaceted understanding of a characteristic, with answers to each question providing complementary insights. Nonetheless, much has changed in the intervening years, and new data call for a more nuanced application of Tinbergen's framework. The anniversary would seem a suitable opportunity to reflect on the four questions and evaluate the scientific work that they encourage.

Section snippets

Origins of Tinbergen's questions

In a famous paper dedicated to Konrad Lorenz on his 60th birthday, Niko Tinbergen [1] recognised that biologists working on behaviour focus on different types of problem. Some want to know, for instance, how the expression of a particular character is controlled, whereas others want to know how it benefits the organism. Tinbergen pointed out that four fundamentally different types of problem are raised in biology, which he listed as ‘survival value’, ‘ontogeny’, ‘evolution’, and ‘causation’.

What is it for?

Tinbergen [1] devoted a substantial proportion of his paper to investigation of the function of a character (what we refer to here as its ‘current utility’), because he felt that this aspect of ethology had been neglected. Tinbergen's own research group showed how hypotheses about current utility could be tested through experimentation [11], and he would no doubt have been delighted to see how his pioneering work has blossomed into one of the most vigorous and productive fields of behavioural

How did it develop?

Although Tinbergen is credited with stimulating research into behavioural development through his inclusion of ontogeny in his list of problems, he himself carried out little research on this topic. However, developmental ethologists and psychobiologists (such as Gottlieb, Hinde, Hogan, Kruijt, Marler, and ten Cate) formed strong links, leading to productive investigations of topics such as attachment, filial and sexual imprinting, and bird song 26, 27.

However, critical issues have arisen over

How did it evolve?

The past 50 years have witnessed major developments in understanding the evolution of behaviour, derived through the development of sophisticated theoretical tools, such as comparative statistical methods used to construct phylogenies, as well as experimental investigations of natural and artificial selection. Despite this progress, of all the problems identified by Tinbergen, evolutionary questions have been the subject of most discussion. Tinbergen thought that the main issue was to do with

How does it work?

In 1963, Tinbergen lamented the plurality of fields that explored the mechanistic bases of behaviour, and called for a multilevel analysis ‘ranging from the behaviour of the individual and even of supra-individual societies all the way down to Molecular Biology’ ([1] p. 416; see also [60]). The links between the levels of analysis remained relatively tenuous for many years, but more recently enormous strides have been made in understanding the molecular, neurobiological, and hormonal bases of

Inter-relations between the four problems

Tinbergen's questions are not the only questions that can usefully be asked about behaviour and, over the years, many candidate ‘fifth questions’ have been proposed (Box 1). Nonetheless, Tinbergen's questions retain a deserved prominence. Tinbergen regarded his distinctions as being pragmatic, but in many respects they are also logical: answers to any one of Tinbergen's questions cannot be regarded as also answering another [65].

The importance of this issue does not imply that each of

Concluding remarks

The above considerations lead us to several practical recommendations (Box 2), designed to retain the spirit of Tinbergen's objectives but update them in the light of insights garnered over the past 50 years. Tinbergen saw a great advantage in addressing all four of his problems. He wrote: ‘a comprehensive, coherent science of Ethology has to give equal attention to each of them and to their integration’ ([1], p. 411). Therefore, he would have been disappointed that much behavioural work

Acknowledgements

Research supported in part by an ERC Advanced grant to K.N.L. We are grateful to Melissa Bateson, Neeltje Boogert, Gillian Brown, Cara Evans, Tom Morgan, Luke Rendell, Peter Slater, Chris Templeton, and Carel ten Cate for helpful comments on earlier drafts of this manuscript.

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