Adaptability and evolution.

The capacity of organisms to respond in their own lifetimes to new challenges in their environments probably appeared early in biological evolution. At present few studies have shown how such adaptability could influence the inherited characteristics of an organism's descendants. In part, this has been because organisms have been treated as passive in evolution. Nevertheless, their effects on biological evolution are likely to have been important and, when they occurred, accelerated the pace of evolution. Ways in which this might have happened have been suggested many times since the 1870s. I review these proposals and discuss their relevance to modern thought.

Robustness and plasticity in development.

Like the game of chess, the overall development of human behavior is highly regulated, and also many finer points of any particular individual life depend on early moves. The robust mechanisms that make species different from each other also impact processes that make individuals distinct from one another. Children both influence their environment and are influenced by it. As the development of any particular skill depends upon the contribution of particular environmental inputs at particular times, environmental variability can dramatically change the process. Development is seldom a linear process: while large environmental changes sometimes have little effect on developmental outcomes, small changes can have enormous (if not always immediate) effects. If we are to unravel these complex interdependencies, we must study the interplay among developmental factors that generates change. WIREs Cogn Sci 2017, 8:e1386. doi: 10.1002/wcs.1386 For further resources related to this article, please visit the WIREs website.

Thirty years of collaboration with Gabriel Horn.

All the collaborative work described in this review was on the process of behavioural imprinting occurring early in the life of domestic chicks. Finding a link between learning and a change in the brain was only a first step in establishing a representation of the imprinting object. A series of overlapping experiments were necessary to eliminate alternative explanations. Once completed, a structure, the intermediate and medial mesopallium (IMM), was found to be strongly linked to the formation of a neural representation of the object used for imprinting the birds. With the site identified, lesion experiments showed that it was necessary for imprinting but not associative learning. Also the two sides of the brain responded differently with the left IMM acting as a permanent store and the right side acting as a way station to other parts of the brain. The collaborative work led to many studies by Gabriel Horn with others on the molecular and cellular bases of imprinting, and also to neural net modelling and behavioural studies with me on the nature of category formation in intact animals.

The biology of developmental plasticity and the Predictive Adaptive Response hypothesis.

Many forms of developmental plasticity have been observed and these are usually beneficial to the organism. The Predictive Adaptive Response (PAR) hypothesis refers to a form of developmental plasticity in which cues received in early life influence the development of a phenotype that is normally adapted to the environmental conditions of later life. When the predicted and actual environments differ, the mismatch between the individual's phenotype and the conditions in which it finds itself can have adverse consequences for Darwinian fitness and, later, for health. Numerous examples exist of the long-term effects of cues indicating a threatening environment affecting the subsequent phenotype of the individual organism. Other examples consist of the long-term effects of variations in environment within a normal range, particularly in the individual's nutritional environment. In mammals the cues to developing offspring are often provided by the mother's plane of nutrition, her body composition or stress levels. This hypothetical effect in humans is thought to be important by some scientists and controversial by others. In resolving the conflict, distinctions should be drawn between PARs induced by normative variations in the developmental environment and the ill effects on development of extremes in environment such as a very poor or very rich nutritional environment. Tests to distinguish between different developmental processes impacting on adult characteristics are proposed. Many of the mechanisms underlying developmental plasticity involve molecular epigenetic processes, and their elucidation in the context of PARs and more widely has implications for the revision of classical evolutionary theory.

Evolution, epigenetics and cooperation.

Explanations for biological evolution in terms of changes in gene frequencies refer to outcomes rather than process. Integrating epigenetic studies with older evolutionary theories has drawn attention to the ways in which evolution occurs. Adaptation at the level of the gene is givingway to adaptation at the level of the organism and higher-order assemblages of organisms. These ideas impact on the theories of how cooperation might have evolved. Two of the theories, i.e. that cooperating individuals are genetically related or that they cooperate for self-interested reasons, have been accepted for a long time. The idea that adaptation takes place at the level of groups is much more controversial. However, bringing together studies of development with those of evolution is taking away much of the heat in the debate about the evolution of group behaviour.

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

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.

The impact of the organism on its descendants.

Historically, evolutionary biologists have taken the view that an understanding of development is irrelevant to theories of evolution. However, the integration of several disciplines in recent years suggests that this position is wrong. The capacity of the organism to adapt to challenges from the environment can set up conditions that affect the subsequent evolution of its descendants. Moreover, molecular events arising from epigenetic processes can be transmitted from one generation to the next and influence genetic mutation. This in turn can facilitate evolution in the conditions in which epigenetic change was first initiated.

An evaluation of the concept of innateness.

The concept of innateness is often used in explanations and classifications of biological and cognitive traits. But does this concept have a legitimate role to play in contemporary scientific discourse? Empirical studies and theoretical developments have revealed that simple and intuitively appealing ways of classifying traits (e.g. genetically specified versus owing to the environment) are inadequate. They have also revealed a variety of scientifically interesting ways of classifying traits each of which captures some aspect of the innate/non-innate distinction. These include things such as whether a trait is canalized, whether it has a history of natural selection, whether it developed without learning or without a specific set of environmental triggers, whether it is causally correlated with the action of certain specific genes, etc. We offer an analogy: the term 'jade' was once thought to refer to a single natural kind; it was then discovered that it refers to two different chemical compounds, jadeite and nephrite. In the same way, we argue, researchers should recognize that 'innateness' refers not to a single natural kind but to a set of (possibly related) natural kinds. When this happens, it will be easier to progress in the field of biological and cognitive sciences.

Nick Thompson on design.

Most biologists are struck by the many close fits between organisms' characteristics and the environments which they inhabit. The adaptations look as they have been designed, but their origins are explained in terms of Charles Darwin's natural selection. Nick Thompson, to whom this essay is dedicated, frequently wrote about design and insisted that the concept should not treated in the same way as the notion of current utility, the idea that an organism's trait increases its chances of survival and reproductive success. He was right, but sadly the whole idea of design has been appropriated by the creationists seeking scientific respectability for their extremist nonsense. As a result biologists are now shy about using the term.

Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behavior in mice.

Across species there is evidence that the quality of the early social environment can have a profound impact on neurobiology and behavior. In the present study we explore the effect of communal rearing conditions (three dams with three litters per cage) during the postnatal period on offspring (F1) and grand-offspring (F2) anxiety-like and maternal behavior in Balb/c mice. Females rearing pups in communal nests exhibited increased levels of postpartum maternal care and communal rearing was found to abolish sex-differences in weaning weights. In adulthood, communally reared offspring were observed to display reduced anxiety-like behavior when placed in a novel environment. When rearing their own offspring under standard conditions, communally reared females demonstrated higher levels of motivation to retrieve pups, built higher quality nests, and exhibited higher levels of postpartum care compared to standard reared females. When exposed to an intruder male, communally reared females were more subordinate and less aggressive. F2 offspring of communally reared females were observed to engage in reduced anxiety-like behavior, have larger litter sizes and an increased frequency of nursing on PND 1. Analysis of neuropeptide receptor levels suggest that a communal rearing environment may exert sustained effects on behavior through modification of oxytocin and vasopressin (V1a) receptor densities. Though Balb-C mice are often considered "socially-incompetent" and high in anxiety-like behavior, our findings suggest that through enrichment of the postnatal environment, these behavioral and neuroendocrine deficits may be attenuated both within and across generations.