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.

Developmental plasticity and human health.

Many plants and animals are capable of developing in a variety of ways, forming characteristics that are well adapted to the environments in which they are likely to live. In adverse circumstances, for example, small size and slow metabolism can facilitate survival, whereas larger size and more rapid metabolism have advantages for reproductive success when resources are more abundant. Often these characteristics are induced in early life or are even set by cues to which their parents or grandparents were exposed. Individuals developmentally adapted to one environment may, however, be at risk when exposed to another when they are older. The biological evidence may be relevant to the understanding of human development and susceptibility to disease. As the nutritional state of many human mothers has improved around the world, the characteristics of their offspring--such as body size and metabolism--have also changed. Responsiveness to their mothers' condition before birth may generally prepare individuals so that they are best suited to the environment forecast by cues available in early life. Paradoxically, however, rapid improvements in nutrition and other environmental conditions may have damaging effects on the health of those people whose parents and grandparents lived in impoverished conditions. A fuller understanding of patterns of human plasticity in response to early nutrition and other environmental factors will have implications for the administration of public health.

Natural variations in postpartum maternal care in inbred and outbred mice.

The role of maternal care in mediating variation in offspring phenotype has been examined in the rat and demonstrates that mother-infant interactions are critical for inducing long-term changes in behavior. Though phenotypic differences between mice strains are often attributed to genetic factors, the influence of early maternal environment has not been extensively explored. To understand maternal influence on phenotype in mice, we must first explore the nature of differences in behavior. In the present study, we examine aspects of maternal care differentiating mice strains and explore the relationship between postpartum behavior and measures obtained by a standard test of maternal responsivity (Retrieval Test). We compared inbred 129Sv (n=25), C57BL/6J (n=23), and outbred Swiss (n=23) lactating female mice. Swiss females had shorter latencies to retrieve and crouch over pups (P<.01), whereas 129Sv females had shorter latencies to nestbuild (P<.05). Conversely, observations of homecage behavior indicate that 129Sv females nestbuild less frequently. 129Sv females also engaged in very low levels of pup licking/grooming (P<.001) and long periods of nursing/contact (P<.05) with pups compared to C57BL/6J and Swiss females. Temporal analysis suggests that the magnitude of these differences varies both within and between days. No significant correlations were found between any aspect of maternal responsivity and postpartum behavior. These results illustrate that through detailed analysis of maternal behavior in mice, variations between strains can be observed. These variations represent strain specific strategies for promoting growth and survival of offspring during infancy that may also mediate "epigenetic" differences in phenotype in adulthood.

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.

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.

Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies.

Early experience has a particularly great effect on most organisms. Normal development may be disrupted by early environmental influences; individuals that survive have to cope with the damaging consequences. Additionally, the responses required to cope with environmental challenges in early life may have long-term effects on the adult organism. A further set of processes, those of developmental plasticity, may induce a phenotype that is adapted to the adult environment predicted by the conditions of early life. A mismatch between prediction and subsequent reality can cause severe health problems in those human societies where economic circumstances and nutrition are rapidly improving. Understanding the underlying mechanisms of plasticity is, therefore, clinically important. However, to conduct research in this area, developmental plasticity must be disentangled from disruption and the adverse long-term effects of coping. The paper reviews these concepts and explores ways in which such distinctions may be made in practice.

The return of the whole organism.

The long trend towards analysis at lower and lower levels is starting to reverse. The new integrative studies must make use of the resources uncovered by molecular biology but should also use the characteristics of whole organisms to measure the outcomes of developmental processes. Two examples are given of how movement between levels of analysis is being used with increasing power and promise. The first is the study of behavioural imprinting in birds where many of the molecular and neural mechanisms involved have been uncovered and are now being integrated to explain the behaviour of the whole animal. The second is the triggering during sensitive periods in early life by environmental events of one of several alternative modes of development leading to different phenotypes. A renewed focus on the whole organism is also starting to change the face of evolutionary biology. The decision-making and adaptability of the organism is recognized an important driver of evolution and is increasingly seen as an alternative to the gene-focused views.

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.

William Bateson: a biologist ahead of his time.

William Bateson coined the term genetics and, more than anybody else, championed the principles of heredity discovered by Gregor Mendel. Nevertheless, his reputation is soured by the positions he took about the discontinuities in inheritance that might precede formation of a new species and by his reluctance to accept, in its full-blooded form, the view of chromosomes as the controllers of individual development. Growing evidence suggests that both of these positions have been vindicated. New species are now thought to arise as the result of genetic interactions, chromosomal rearrangements, or both, that render hybrids less viable or sterile. Chromosomes are the sites of genes but genes move between chromosomes much more readily than had been previously believed and chromosomes are not causal in individual development. Development, like speciation, requires an understanding of the interactions between genes and the interplay between the individual and its environment.

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.