Tinbergen's four questions

• behavioural adaptive functions
• phylogenetic history; and the proximate explanations
• underlying physiological mechanisms
• ontogenetic/developmental history.

Four categories of questions and explanations

When asked about the purpose of sight in humans and animals, even elementary-school children can answer that animals have vision to help them find food and avoid danger (function/adaptation). Biologists have three additional explanations: sight is caused by a particular series of evolutionary steps (phylogeny), the mechanics of the eye (mechanism/causation), and even the process of an individual's development (ontogeny). This schema constitutes a basic framework of the overlapping behavioural fields of ethology, behavioural ecology, comparative psychology, sociobiology, evolutionary psychology, and anthropology. The first three had been identified in around 350 BC by the Greek philosopher Aristotle in his biology, and formalised in the 20th century by Julian Huxley. Tinbergen gave only the fourth question, as Aristotle's formulation failed to distinguish between survival value and evolutionary history. The fourth question helped to resolve this problem.

Evolutionary (ultimate) explanations

First question: Function (adaptation)

Darwin's theory of evolution by natural selection is the only scientific explanation for why an animal's behaviour is usually well adapted for survival and reproduction in its environment. However, claiming that a particular mechanism is well suited to the present environment is different from claiming that this mechanism was selected for in the past due to its history of being adaptive.

The literature conceptualizes the relationship between function and evolution in two ways. On the one hand, function and evolution are often presented as separate and distinct explanations of behaviour. On the other hand, the common definition of adaptation is a central concept in evolution: a trait that was functional to the reproductive success of the organism and that is thus now present due to being selected for; that is, function and evolution are inseparable. However, a trait can have a current function that is adaptive without being an adaptation in this sense, if for instance the environment has changed. Imagine an environment in which having a small body suddenly conferred benefit on an organism when previously body size had had no effect on survival. A small body's function in the environment would then be adaptive, but it would not become an adaptation until enough generations had passed in which small bodies were advantageous to reproduction for small bodies to be selected for. Given this, it is best to understand that presently functional traits might not all have been produced by natural selection. The term "function" is preferable to "adaptation", because adaptation is often construed as implying that it was selected for due to past function. This corresponds to Aristotle's final cause.

Second question: Phylogeny (evolution)

Evolution captures both the history of an organism via its phylogeny, and the history of natural selection working on function to produce adaptations. There are several reasons why natural selection may fail to achieve optimal design (Mayr 2001:140–143; Buss et al. 1998). One entails random processes such as mutation and environmental events acting on small populations. Another entails the constraints resulting from early evolutionary development. Each organism harbors traits, both anatomical and behavioural, of previous phylogenetic stages, since many traits are retained as species evolve.

Reconstructing the phylogeny of a species often makes it possible to understand the "uniqueness" of recent characteristics: Earlier phylogenetic stages and (pre-) conditions which persist often also determine the form of more modern characteristics. For instance, the vertebrate eye (including the human eye) has a blind spot, whereas octopus eyes do not. In those two lineages, the eye was originally constructed one way or the other. Once the vertebrate eye was constructed, there were no intermediate forms that were both adaptive and would have enabled it to evolve without a blind spot.

It corresponds to Aristotle's formal cause.

Proximate explanations

Third question: Mechanism (causation)

Some prominent classes of Proximate causal mechanisms include:

• The brain: For example, Broca's area, a small section of the human brain, has a critical role in linguistic capability.
• Hormones: Chemicals used to communicate among cells of an individual organism. Testosterone, for instance, stimulates aggressive behaviour in a number of species.
• Pheromones: Chemicals used to communicate among members of the same species. Some species (e.g., dogs and some moths) use pheromones to attract mates.

In examining living organisms, biologists are confronted with diverse levels of complexity (e.g. chemical, physiological, psychological, social). They therefore investigate causal and functional relations within and between these levels. A biochemist might examine, for instance, the influence of social and ecological conditions on the release of certain neurotransmitters and hormones, and the effects of such releases on behaviour, e.g. stress during birth has a tocolytic (contraction-suppressing) effect.

However, awareness of neurotransmitters and the structure of neurons is not by itself enough to understand higher levels of neuroanatomic structure or behaviour: "The whole is more than the sum of its parts." All levels must be considered as being equally important: cf. transdisciplinarity, Nicolai Hartmann's "Laws about the Levels of Complexity."

It corresponds to Aristotle's efficient cause.

Fourth question: Ontogeny (development)

Ontogeny is the process of development of an individual organism from the zygote through the embryo to the adult form.

In the latter half of the twentieth century, social scientists debated whether human behaviour was the product of nature (genes) or nurture (environment in the developmental period, including culture).

An example of interaction (as distinct from the sum of the components) involves familiarity from childhood. In a number of species, individuals prefer to associate with familiar individuals but prefer to mate with unfamiliar ones (Alcock 2001:85–89, Incest taboo, Incest). By inference, genes affecting living together interact with the environment differently from genes affecting mating behaviour. A simple example of interaction involves plants: Some plants grow toward the light (phototropism) and some away from gravity (gravitropism).

Many forms of developmental learning have a critical period, for instance, for imprinting among geese and language acquisition among humans. In such cases, genes determine the timing of the environmental impact.

A related concept is labeled "biased learning" (Alcock 2001:101–103) and "prepared learning" (Wilson, 1998:86–87). For instance, after eating food that subsequently made them sick, rats are predisposed to associate that food with smell, not sound (Alcock 2001:101–103). Many primate species learn to fear snakes with little experience (Wilson, 1998:86–87).

It corresponds to Aristotle's material cause.