Tinbergen's Four Questions
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Randolph M. Nesse
The University of Michigan
426 Thompson St, Room 5261
Ann Arbor, MI 48104
(734) 764-6593
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nesse@umich.edu
Contact information until May 7, 2003
Randolph M. Nesse, M.D.
Dept. Anthropology
University College London
Malet Court
London WC1E 6BT UK
Phone: 44 (0)20 7679 3381
Fax: 44 (0)20 7679 7728
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In 1963, to honor Konrad Lorenz’s 60th birthday, Nico Tinbergen wrote an article
titled “On the aims and methods of ethology.” On the 40th anniversary of its
publication, the conceptual foundation it provides is more influential than ever, not
only for animal behavior but for biology in general. The paper is organized according
to Tinbergen’s now-famous Four Questions. He called them “causation, survival
value, ontogeny and evolution.” Now they are more commonly referred to as
mechanism, selective advantage, ontogeny and phylogeny.
As Dewsbury has noted, such categories are never completely new. In 1961, Mayr
clarified the distinction between proximate causes of structures and functional
mechanisms in individuals as contrasted with evolutionary (“ultimate”) causes of
traits in a population. Tinbergen’s Four Questions augment this dichotomy by calling
attention to the differences between explanations that address a slice in time as
compared to a historical sequence. Perhaps equally valuable is his emphasis on the
independence of each question. They are not competing alternatives but four
complementary components of a complete biological explanation. Confusion on this
point still gives rise to much useless controversy.
Questions about Mechanism have also been called “causal,” “structural,” “proximate”
or “immediate.” This question actually has incorporated two somewhat different
kinds of inquiry— those about intrinsic mechanisms and the body’s structures and
how they work to carry out their functions, and those in which behavior is explained
by extrinsic factors that immediately precede a behavior or other response. Both
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inquiries provide explanations of individuals based on mechanisms and current
circumstances. The other three questions all explain the origins of the mechanisms.
The second proximate question is about Ontogeny, the explanation of traits in terms of
the mechanisms that transform precursors into their successors in developmental
sequences. Mechanism and ontogeny help to explain each other; all developmental
transitions needs mechanistic explanations and all structures need developmental
explanations.
Evolutionary questions ask why a population is the way it is, in the sense of “How
come?” More specifically, they describe the forces, natural selection and others,
which account for a trait’s transformation from its phylogenetic precursors. Selective
Advantage was called “survival value” by Tinbergen, who wrote just prior to
recognition of the importance of reproductive success. These questions have also
been called “functional,” with much resulting confusion because Mayr used the same
word to refer to the area of biology that studies structure and mechanisms. The core
concept is adaptive utility that gives a fitness advantage. Of course, it is not the trait
itself that is preserved, but only a DNA sequence. In this sense, questions about
Selective Advantage are, as Mayr noted, fundamentally about why this species has its
particular sequence of DNA. Agreement on methods for testing hypotheses about
adaptation continues to be elusive, but there is growing recognition that the applicable
research strategies—the comparative method, assessment of design for a function,
experimental perturbation of adaptive mechanisms, and observing selection—are
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quite different from the experimental methods that are the mainstay in proximate
biology.
Questions about Phylogeny address the evolutionary history of a trait or a species.
Every attribute, from a Hox gene to a peacock’s tail has an evolutionary history, with
precursors varying by mutation and shaped by selection and drift to the observed
form. The focus has expanded from paleontology to new areas of paleobiology
including methods for inferring phylogeny from genetic sequences and other rapid
advances at the intersection between evolutionary and developmental biology.
Tinbergen’s Four Questions are not a panacea for preventing conceptual confusion in
biology. They do, however, provide a vital framework of enduring utility for
clarifying research questions and preventing useless controversy.
Acknowledgements Thanks to Donald Dewsbury for valuable comments on a draft.
Correspondence and Requests for materials should be addressed to:
Randolph M Nesse
University of Michigan
426 Thompson St, Room 5261
Ann Arbor, MI 48104
nesse@umich.edu
FURTHER READING
Tinbergen, N. On the aims and methods of ethology. Zeitschrift für Tierpsychologie
20, 410-463 (1963).
Dewsbury, D. A. The proximate and the ultimate: past, present and future.
Behavioural Process 46, 189-199 (1999).
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Tinbergen’s
Four
Questions
SLICE IN TIME
An aspect of an
organism at one phase
in the life cycle/one
time in phylogeny
PROXIMATE
EVOLUTIONARY
(causal, immediate, structural)
(distal, ultimate, Darwinian)
Explains what individual
organisms are like and how
bodily mechanisms work
Explains how populations of
organisms came to be
the way they are
MECHANISM
SELECTIVE ADVANTAGE
(structure, physiology, immediate)
(adaptive, functional, survival
value, fitness, teleonomic)
What is the structure, how do
mechanisms work, and how do
they respond to extrinsic factors?
What selective forces in prior
environments explain
characteristics of the trait?
Dewsbury, D. A. On the problems studied in ethology, comparative psychology, and
animal behavior. Ethology 92, 89-107 (1992).
Mayr, E. Cause and effect in biology. Science 134, 1501-1506 (1961).
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HISTORICAL
SEQUENCE
How precursors were
transformed into the
current trait
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ONTOGENY
PHYLOGENY
(developmental)
(evolutionary historical)
What developmental precursors
and mechanisms explain the trait
at this life stage?
What phylogenetic precursors
and mechanisms account for the
trait in this evolutionary epoch?
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