Fetal experience and good adult designa

Biology is the study of complicated things that give the appearance of having been designed for a purpose. This thought has been articulated most clearly in recent years by Richard Dawkins,1 but it has been expressed in various ways for 200 years. A traveller finding a watch on a mountain path would not fail to attribute the quality of its design to human agency. A great British naturalist and theologian, William Paley2 regarded the design he saw everywhere in nature as proof of the existence of God. These days, the design to which Paley referred would instead be attributed by most biologists to blind Darwinian evolution. The form and behaviour of individuals vary within the same species and, in any given set of environmental conditions, some individuals may be better able to survive and reproduce than others because their distinctive characteristics are particularly well suited to those conditions. If their characteristics are inherited, then an ever increasing number of individuals in the population will be better adapted to that environment than was previously the case. Plant and animal breeders have known for years how to select artificially the characteristics which they prized for one reason or another. Darwin called the blind evolutionary process leading to the appearance of good design ‘natural selection’.3 His phrase was popular in the 19th century because it suggested an agent for evolution. These days many biologists prefer to focus on the processes. What generates variation in the first place? What leads to differential survival and reproductive success? What genetic and environmental factors enable individual characteristics to be replicated in subsequent generations? While each of these questions raises separate issues, it is worth keeping in mind the idea of the evolutionary outcome—apparent design. After a fire on the high grassland planes of East Africa, the recently hatched grasshoppers are black instead of being the normal pale yellowish-green. Something has switched the course of their development onto a different track. The grasshopper's colour makes a big difference to the risk that it will be spotted and eaten by a bird as the scorched grassland may remain black for many months after a fire. So matching its body colour to the blackened background is important for its survival. The developmental mechanism for making this switch in body colour is automatic and depends on the amount of light reflected from the ground. If the young grasshoppers are placed on black paper they are black when they moult to the next stage.4 If they are placed on pale paper, however, the moulting grasshoppers are the normal green colour. The grasshoppers actively select habitats with colours that match their own. If the colour of the background changes they can also change their colour at the next moult to match the background, but they are committed to a colour once they reach adulthood. Turtles and crocodiles and some other reptiles commit themselves early in life to developing along one of two different developmental tracks and like grasshoppers, they do so in response to a feature of their environment. Each individual starts life with the capacity to become either a male or a female.5 The outcome depends on environmental temperature during the middle third of embryonic development. If the eggs from which they hatch are buried in sand below 30°C, the young turtles become males. If, however, the eggs are incubated at above 30°C they become females. Temperatures below 30°C activate genes responsible for the production of male sex hormones and male sex hormone receptors. If the incubation temperature is above 30°C, a different set of genes is activated, producing female hormones and receptors instead. It so happens that in alligators the sex determination works the other way around, such that eggs incubated at higher temperatures produce males. (In humans and other mammals, by contrast, the sex of each individual is determined genetically at conception; if it inherits only one X sex chromosome it becomes male.) Each grasshopper and turtle starts life with the capacity to take one of two distinctly different developmental routes—becoming green or black, male or female. A particular feature of the environment determined the path taken by the individual for the rest of its life, and once committed, the individual cannot switch to the other route. Once black as an adult, the grasshopper cannot subsequently change its colour to green, just as a male turtle cannot transform itself into a female. The broad pattern of an individual's social and sexual behaviour may also be determined early in life, with the individual developing along one of two or more qualitatively different tracks. Many examples are found in the animal kingdom. The caste of a female social insect is determined by her nutrition early in life. The main egg producer of an ant colony, the queen, is part of a teeming nest in which some of her sisters care for her offspring, others forage, yet others clean or mend the nest, and finally other sisters specialize in guarding it.6 The sexual behaviour of some primates can also develop along two or more distinctly different tracks. An adult male gelada baboon, for example, will typically defend and breed with a harem of females. After a relatively brief but active reproductive life, he is displaced by another male and never breeds again. To position himself so that he can acquire and defend a harem, the male must grow rapidly at puberty. He develops the distinctive golden mane of a male in his prime and becomes almost twice the size of the females.7 However, when many such males are present in the social group, an adolescent male may adopt a distinctly different style of reproductive behaviour. He does not develop a mane or undergo a growth spurt. Instead, he remains similar in appearance and size to the females. These small males hang around the big males' harems, sneakily mating with a female when the harem-holder is not paying attention. Since the small, sneaky male never has to fight for females, he is likely to have a longer, if less intense, reproductive life. If he lasts long enough he may even do better in terms of siring offspring than a male who pursues the alternative route of growing large and holding a harem. It is believed that these two different modes of breeding behaviour represent two distinctly different developmental routes, and each male baboon must commit himself to one or other of them before puberty.7 In each of the above cases, the individual animal starts its life with the capacity to develop in a number of distinctly different ways. Like a jukebox, the individual has the potential to play a number of different developmental tunes. But during the course of its life it plays only one tune. The particular developmental tune it plays is triggered by a feature of the environment in which the individual is growing up—whether it be the colour of the ground, the temperature of the sand, the type of food, or the presence of other males. Furthermore, the particular tune emanating from the developmental jukebox is adapted to the conditions in which it is played.8 Many other examples can be given.9,10 The juke-box analogy has its drawbacks because it implies the tune is pre-formed somehow; like everything else, the expressed phenotype has to develop.11 The analogy with ‘programming’12 is even worse because it implies that the environmental trigger contains the instructions for the phenotype that will be expressed. The term ‘imprinting’13,14 has a somewhat similar defect. Perhaps, the best general term for the processes is an old one used in development biology for many years, namely ‘induction’. The implication of many of the phenomena described here is that environmental induction provides a prediction about the conditions of the world which the individual will subsequently inhabit. In mammals the best route for such a forecast may be via the mother. Vole pups born in the autumn have much thicker coats than those born in spring; the cue to produce a thicker coat is provided by the mother before birth.15 The value of preparing in this way for colder weather is obvious. Maternal forecasting by induction is likely to be very important in human biology. Is it the case that people, like grasshoppers or baboons, are conceived with the capacity to play a number of qualitatively different developmental tunes—in other words, to live alternative lives? Each of us started life with the capacity to live many different lives, but each of us lives only one. In one sense individual humans are obviously bathed in the values of their own particular culture and become committed by their early experience to behaving in one of many possible ways. Differences in early linguistic experience, for example, have obvious and long-lasting effects. By the end of a typical high school education, a young American will probably know about 50 000 different words.16 The words are different from those used by a Russian of the same age. In general, individual humans imbibe the particular characteristics of their culture by learning (often unwittingly) from older people. When environmental conditions induce a particular developmental route in animals, the mechanisms involved are likely to be different; learning may not enter into the picture at all. Is it possible that some aspects of human development are triggered by the environment, as though the individual were a jukebox? Was each of us conceived with the capacity to develop along a number of different tracks—to live a number of distinctly different sorts of life? And does the environment trigger the particular developmental track that each of us follows? The now famous series of studies, led by David Barker, assessed people across their entire lifespan from birth to death.17 This work has lent strength to the suggestion that human development may also involve environmental cues that prepare the individual for a particular sort of environment. Those men who had had the lowest body-weights at birth and at one year of age were most likely to die from cardiovascular disease later in life. Those born as the heaviest babies enjoyed a much reduced risk of dying from cardiovascular It was only the for the as a the risk for the babies was above other words, than that for the who had been small babies were also more likely to from such as and in adulthood. 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