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Behaviour, Development and Evolution

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Patrick Bateson

10. Adaptability in Evolution

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1Compelling examples of the interplay between genes and the environment may be found throughout the animal and plant kingdoms (see Chapter 8). Genetically identical individuals may develop in different ways, depending on environmental cues they received when they were young.

2Well-meaning attempts to break out of the nature-nurture straitjacket have often resulted in a bewildering portrayal of development as a process of impenetrable complexity. Indeed, development seemed so unfathomably complex to eighteenth-century biologists that they believed that it must depend on supernatural guidance. On the surface the processes involved in behavioural development do indeed look forbiddingly complicated.

3Order underlies even those learning processes that make individuals different from each other. Knowing something of the underlying regularities in development does bring an understanding of what happens to the child as it grows up. The ways in which learning is structured, for instance, affect how the child makes use of environmental contingencies and how the child classifies perceptual experience. Yet predicting precisely how an individual child will develop in the future from knowledge of the developmental rules for learning is no easier than predicting the course of a chess game. The rules influence the course of a life, but they do not determine it. Like chess players, children are active agents. They influence their environment and are in turn affected by what they have done. Furthermore, children’s responses to new conditions will, like chess players’ responses, be refined or embellished as they gather experience. Sometimes normal development of a particular ability requires input from the environment at a particular time; what happens next depends on the character of that input. The upshot is that, despite their underlying regularities, developmental processes seldom proceed in straight lines. Big changes in the environment may have no effect whatsoever, whereas some small changes may have big effects.

4A more general point is that the development of individuals is readily perceived as an interplay between them and their environment. The current state influences which genes are expressed, and gene expression depends on the animal’s social and physical world. Individuals are then seen as choosing and changing the conditions to which they are exposed. The question, though, is within what limits will the developmental systems, dynamic as they are, produce the same result. A developmental system that had been sufficiently perturbed would be expected to lead to a markedly different outcome.

5Sometimes the perturbations produced by the new set of conditions may be such that developmental processes generate maladaptive outcomes — such as flippers instead of arms when the human embryo had been exposed to thalidomide. If conditions are changed enough, developmental stability is no longer maintained. The biological equivalent of an earthquake occurs and the appearance of organisms may suddenly change. If such a change occurs early in development, the effects may ramify and generate a radically different outcome. Even spontaneously expressed behaviour is only buffered from environmental conditions within certain limits. Changes in conditions may kill the animal, but they can also open up important new avenues for subsequent evolutionary change. That is why knowledge of development impinges on studies of evolution and why genetic determinism has stultified thought about the nature of evolution.

  • 1 The mantra among most evolutionary biologists used to be that evolution involves changes in the fre (...)

6Studies of development and evolution are logically distinct. Knowledge of how a particular automobile has been assembled does not tell us anything about the evolution of automobile design and the same is true of living organisms. The outcome of evolutionary processes is expressed in an individual’s development. Furthermore, Darwinian evolution acts on the outcome of developmental processes.1 The growing awareness of the emergent properties of developing systems does, therefore, have implications for evolutionary biologists who traditionally have entertained rather simple notions of what happens in development. Considering all the factors that are involved in development, including the genes, emphasises the benefits of adopting a systems approach.

7The likelihood that one group of factors is exclusively important in development and evolution would seem odd to gardeners who have a good understanding of how the character of the soil, the presence of symbiotic activity of fungae next to the roots, the amount of fertilizer supplied, and so forth, all affect how well the plant thrives. Similarly sensitive dog and cat breeders, irrespective of the breed, know how important is the early age of socialisation to the pet’s friendliness to humans. People who cook for themselves, know how important is the choice of ingredients that will work well together and on the length and temperature of cooking.

8Examples of condition-dependent development do not pose any problems for evolutionary theory, even though they should give pause to those who search for universals within a given species. From a Darwinian standpoint, the development of characteristics that are appropriate to the circumstances in which the individual finds itself makes a great deal of sense.

9The many examples of conditional responses to the environment illustrate an important aspect of development that has intriguing implications for humans. Do people have the capacity to live alternative lives? Individual humans are 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. In general, individual humans imbibe the particular characteristics of their culture by learning from older people even if unwittingly.

10When environmental conditions influence a particular developmental route in animals, the mechanisms involved are likely to be different; learning may not enter into the picture at all. Even so, is it possible that some aspects of human development are triggered by the environment? Was each individual conceived with the capacity to develop along a number of different tracks each of which is adapted to circumstances in which the individual may find itself? People who grow up in impoverished conditions tend to have a smaller body size, a lower metabolic rate and a reduced level of behavioural activity. These responses to early deprivation are generally regarded as pathological — just three of the many damaging consequences of poverty. The long-term effects on health of a low birth weight may simply be by-products of the continuing social and economic conditions that stunted growth in the first place. Ignorance and shortage of money make the prevention and treatment of disease more difficult; overcrowding, bad working conditions and poverty produce psychological stress and increase the risk of infection. People with little money have poorer diets, and adverse social or physical factors that foster depression and hopelessness increase the risks of disease. In industrialised nations the poor and the unemployed have more illnesses and die sooner than the affluent.

  • 2 Gluckman, P.D., Hanson, M.A. & Buklijas, T. (2010), A conceptual framework for the developmental or (...)

11Despite all the well-known effects of poverty, in less extreme conditions they could also be viewed as part of a package of characteristics that are appropriate to the conditions in which the individual grows up — in other words, adaptations to an environment that is chronically short of food, rather than merely the pathological by-products of a bad diet. Having a lower metabolic rate, reduced activity and a smaller body all help to reduce energy expenditure, which can be crucial when food is usually in short supply. To put it simply, they might be adaptations to make the best of a bad job.2

  • 3 Chali, D., Enquselassie F. & Gesese M. (1998), A case-control study on determinants of rickets. Eth (...)

12If this idea is correct, what about those individuals that are born as big babies who end up in an impoverished environment? The evidence is much weaker, but in general it supports the view that people born in affluent conditions are at greater risk during periods of prolonged famine than those who experienced lower levels of nutrition during prenatal development. Children born to affluent parents are more likely to suffer adverse effects if they are starved in adulthood. In concentration camps and the worst prisoner-of-war camps, anecdotal evidence suggests that the physically large individuals died first while at least some of the small individuals survived. In a famine-exposed Ethiopian population, high birth weight was associated with a nine-fold greater risk of rickets.3 Rickets in women severely affects their subsequent reproductive success. It seems likely therefore that humans like so many other animals do respond in ways that are usually appropriate to the conditions in which they started life. These ways can be distinctly different from each other.

  • 4 Bateson, P., Gluckman, P. & Hanson, M., The biology of developmental plasticity and the Predictive (...)

13A series of studies that assessed people across their entire lifespan from birth to death has lent strength to the suggestion that human development involves environmental cues that prepare the individual for a particular sort of environment. Those people 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. They were also more likely to suffer from diseases such as diabetes and stroke in adulthood.4 How do these associations these connections make sense in adaptive terms? Could it be that, in bad conditions, the pregnant woman unwittingly signals to her unborn baby that the environment her child is about to enter is likely to be harsh? Such a weather forecast from the mother’s body could result in her baby being born with adaptations, such as a small body and a modified metabolism, that help it to cope with a shortage of food. If instead the baby finds itself growing up in an affluent industrialised society, it is poorly adapted.

14Charles Darwin’s great theory of the evolution of adaptations found in nature remains as important as ever. Even so, the picture of the external hand of natural selection doing all the work is so compelling that it is easy to regard organisms as if they were entirely passive in the evolutionary process. Of course no biologist would deny that organisms, and animals especially, are active. Even so the notion of ‘selection pressure’ does subtly downplay the role of organisms in the processes of change. When behavioural and developmental issues are joined together with questions about evolution, it becomes easier to perceive how an organism’s behaviour can initiate and direct lines of evolution. Developmental processes do not merely act as constraints, they can make certain types of evolutionary change more likely. The explosion in the study of epigenetics (see Chapter 8) has suggested some ways in which a link between development and evolution might have occurred.

15Proposals about the active involvement of animals in evolution emphasise how their characteristics develop. By contrast, a certain style of evolutionary theory has placed all the emphasis on changes in gene frequencies in the course of evolution, thereby removing the organism from consideration. The justification for this type of theory has been that genes generally survive generation after generation, whereas individual organisms never do. The consequence of such an approach is that, when the effect of a gene on an organism is considered, the gene alone is supposed to determine the outcome.

  • 5 Braun, E. & David, L. (2011), The role of cellular plasticity in the evolution of regulatory novelt (...)

16The advance of epigenetics has awakened interest in the links between development and evolution. The transmitted epigenetic markers across generations could have facilitated genomic change. In most experimental studies, the environmental stimulus producing an epigenetic change is only applied in one generation. Experimentally this may be enough, since research on yeast suggests that an environmental challenge can permanently alter the regulation of genes.5 In natural conditions, the environmental cues that induce epigenetic change may be recurrent and repeat what has happened in previous generations. This recurring effect might have stabilised the developed characteristics until genomic reorganisation had occurred. The induced epigenetic changes that mediate adaptive plasticity might then have biased the sites of subsequent mutation. Variation at these sites may throw up developed characteristics, some of which are adaptive and subject to Darwinian evolution. This is one way in which plasticity leads to evolutionary change.

Behaviour and evolution

  • 6 The importance of the active role of behaviour in evolution is discussed in Bateson, P. (2013), New (...)

17An animal’s behaviour is likely to have affected the course of evolution of its descendants in at least four ways. First, animals make active choices, and the consequences of their choices are often important. Second, animals change the conditions in which they live by altering the physical or the social environment. Third, active animals often expose themselves to new conditions that reveal variability, with some variants more likely to survive than others. Finally, organisms are adaptable and are able to modify their behaviour in response to novel conditions and thereby make further genetic change possible.6

18The role of choice in evolution was clearly recognised by Darwin in his principle of sexual selection. He suggested that members of one sex choose to mate with individuals possessing a prominent feature. One example, the tail of the male peacock, has already been mentioned. Other examples are given in Chapter 9. Mate choice sets up a feedback process so that the act of choice affects the evolution of a characteristic in the chosen individual which subsequently then affects what is chosen in descendants. The postulated process could lead to an evolutionary instability with a runaway character.

  • 7 Michel, A.P. (2010), Widespread genomic divergence during sympatric speciation. PNAS 107.21, 9724–9 (...)

19The crucial agents necessary for this evolutionary process of adaptation driven by choice will generally be elements of the genome, but this is not always the case. In the past the fly Rhagoletis pomonella typically laid its eggs on the fruits of hawthorns.7 Around one hundred and fifty years ago some flies laid their eggs on apples. Their offspring preferred to lay their eggs on apples and the fly has since become a serious pest in USA orchards. The offspring retain through pupation a ‘memory’ of what they have eaten, and when the new generation of adult flies have mated they lay eggs on the particular species of plant they had eaten before metamorphosis. In this case the variation lies in the behaviour of the adult female flies choosing apples on which to lay their eggs, and onward transmission to the next generation is achieved by an imprinting-like mechanism.

20Darwinian evolution operates on characteristics that have developed within a particular set of conditions, many of which are environmental. Apparent design is produced, even when it is at the end of the long and complicated process of development involving many different factors. The environment does not cease to be important for evolution just because it remains constant. Change the environment and the outcome of an individual’s development may be different. If an individual does not inherit its parents’ environment along with their genes and other transmittable factors, it may not be well adapted to the conditions in which it now finds itself. But the altered environmental conditions may throw up variation that was previously hidden, and from that may spring new lines of evolution.

21Changes in environmental conditions might, for instance, be imposed by a catastrophe resulting from Earth’s collision with a comet or asteroid, or by climate change produced by glaciation and the impact of human activities on the planet. Less dramatically, a change in the environment of a given animal might be brought about because it can move, or in the case of many plants, because their seeds are dispersed. Although the migration of animals can be highly adaptive, the possibility of movement into a novel environment raises a key conceptual point in understanding how developmental plasticity and behaviour can drive evolutionary change.

22The organism’s contribution towards creating an environment to which it is best suited (see Chapter 9) should give pause if evolution is considered purely in terms of selection by external forces. By leaving an impact on their physical and social environment, organisms may affect the evolution of their own descendants, quite apart from changing the conditions in which they live themselves. Some of the impact is subtle, such as when a plant sheds its leaves which fall to the ground and changes the characteristics of the soil in which its own roots and those of its descendants grow. Some of the impact is conspicuous such as when beavers dam a river, flood a valley and create a private lake for themselves. It has been suggested that the aquatic environment created by the beavers led them to evolve adaptations such as webbed feet that facilitated swimming. The hypothesis is plausible because none of the beaver’s nearest relatives, the true gophers and kangaroo rats, have webbed feet. These ideas about the impact organisms on their environment have been developed extensively.

  • 8 Humphrey, N. (1986), The Inner Eye. London: Faber & Faber.

23The effect of behavioural control on evolutionary change could be especially great when the social environment is a major component of the challenges faced by animals. The result would be that individuals evolve to understand and predict what other members of their social group are about to do. They become better able to compete with others that do not have this ability. If individuals compete with each other within a social group and the result of the competition depends in part on each individual’s capacity to predict what the other will do, the evolutionary outcome might easily acquire a run-away property with the intellectually most advanced individuals driving others in the course of evolution to behave in the same way. Such an explanation, which has been developed eloquently by Nick Humphrey, would fit in with the increase in cranial capacity of humans, assuming that cranial capacity and intellectual ability are correlated.8

Nick Humphrey. Photo by LittleHow (2010), Wikipedia, https://commons.wikimedia.org/​wiki/​File:Nick_Humphrey.jpg, CC BY-SA 3.0.

24Active control and manipulation of the environment occurs in play. Extended parental care found in birds and mammals may have provided the lift-off for the evolution of increasingly elaborate play with different beneficial outcomes. The surplus energy available to the young might have created optimal conditions for the evolution of the initial appearance of play behaviour. As discussed in Chapter 9 active engagement with the environment has great benefits, because the world is examined from different angles. Such engagement helps to construct a working knowledge of the environment: recognition of objects, understanding what leads to what, discovering that things are found when stones are turned over and the world is rearranged, learning what can and cannot be done with others. All these discoveries are real benefits for the individual, enhancing neural processing, physical fitness, behavioural coordination, and behavioural flexibility.

25Those individuals that play more have a putative advantage over the others. In effect they go through a period of training that perfects the behaviour they will need when adult. Those of the non-playful individuals’ offspring that behave like the playful individuals are more likely to survive and, by degrees, the whole population plays more except when play has over-riding costs. If some individuals are able to profit in ways other than merely improving their motor skills during play, the evolutionary movement towards greater complexity will continue. The more playful individuals might, for example, become more aware of environmental contingencies than others and gain advantage by doing so. Once again this drives the evolution of the same abilities in the rest of the population.

26The next step in evolution could, among other things, have led to the ability to generate novel behaviour that would have provided the basis for creativity and innovation. Creative people perceive new relations between thoughts, or things, or forms of expression. They are able to combine them into new forms, connecting the seemingly unconnected. Where does such an evolutionary process stop? Presumably the costs of evolving new forms of behaviour or the sheer difficulties of doing so become limiting.

27The effects of a new set of conditions lead either to immediate death or to an appropriate response to the challenge. Initially the response is not inherited, and differential survival of different genotypes may arise from subsequent differences in the ease with which the new character is expressed spontaneously. An unstable evolutionary process could be generated by spontaneous alterations in the genome, but the likelihood of this happening diminishes with the number of components in a response necessary to produce an overall change. The adaptability of the individuals allows by contrast the evolutionary process to occur piecemeal.

28Adaptability driving evolution could start operating when a group of organisms respond appropriately to a change in environmental conditions. The modification of form or behaviour occurs generation after generation under the changed conditions, but the modification will not be inherited. Any genetic variation in the ease of expression of the modified characteristic is liable to favour those individuals that express it most readily and with least cost. Consequently, an inherited predisposition to express the modification will tend to evolve. The longer the evolutionary process continues, the more frequent will be such a predisposition. The process starts through learning or some other form of plastic modification within individuals, but this paves the way for a longer-term change in the genome.

29In principle, then, behaviour patterns that were initially acquired through the animal’s adaptability could be expressed spontaneously, without employing such plasticity, in subsequent generations. It might be argued that spontaneously expressing a behaviour pattern that had been learned in previous generations could be costly if it means that the animal loses its ability to learn. The argument is not cogent when applied to big-brained animals like birds and mammals with multiple parallel pathways for learning. In these animals, the loss of capacity to learn in one way has no effect on the capacity to learn in other ways.

30Adaptability can accelerate the rate at which challenges set by the environment can be met. The effect of plasticity on evolution may have become increasingly powerful as animals, in particular, became more complex. Elements could be recombined in different ways to perform different functions. This evolutionary process could lead to the establishment of increasingly elaborate organization and patterns of behaviour. When such complexity entails a greater ability to discriminate between different features of the environment or a greater ability to manipulate the environment, the organism will benefit and become more likely to survive and reproduce in the face of multiple challenges during its lifetime. A new adaptation would emerge in evolution when the accumulated effects of genomic reorganization altered the organism’s characteristics. Although these effects are specific to the new function, existing parts of the body’s characteristics could also be recruited for this function. Plasticity would promote much more rapid genetic evolution of complex sets of adaptive systems than could be accomplished by changes in the genome. This occurs as previously plastic elements are replaced by inherited elements and the evolving organism is able to replace through its plasticity missing elements in subsequent systems. The exposure to novel environments would be likely to lead to the subsequent evolution by means of classical Darwinian processes of morphological, physiological and biochemical adaptations to those niches.

  • 9 Foster, S.A. et al. (2015), Evolutionary influences of plastic behavioral responses upon environmen (...)

31One case of what can happen when an animal is adaptable has been provided by the three-spine stickleback after moving from a marine to a freshwater environment and then occupying the deep water of lakes or shallow fresh water.9 It was able to adapt and then developed characteristics that distinguished it from its marine ancestors and which were specialized for the environment into which had moved. Shallow water males have striking red bellies involved in courtship whereas those in deep water, which is dark, do not.

  • 10 Beall, C.M. (2007), Two routes to functional adaptation: Tibetan and Andean high-altitude natives. (...)

32Adaptability to new conditions may be physiological, such as coping with high altitudes by enhancing the oxygen carrying capacity of the blood. Humans living at low altitudes can usually cope when mountaineering, but over many generations this adaptability was followed by inherited genomic change which may take different forms. In the course of evolution people living in the Andes have developed a different response from those living in the Himalayas.10

33An important empirical demonstration of adaptability driving evolutionary change is that of the house finch. This species is endemic in the western parts of the USA. Some individuals were collected and taken east to New York but were quickly released when the collector realized that he might be prosecuted. The birds adapted and spread north to Canada.

  • 11 Badyaev, A.V. (2009), Evolutionary significance of phenotypic accommodation in novel environments: (...)

34The same species has spontaneously moved north into Montana where it has been intensively studied. After a period involving a great deal of plasticity in a new environment, the house finch populations spontaneously expressed the physiological characteristics that best fitted them to their new habitats without the need for developmental plasticity. Initially the adaptive onset of the time of incubation that occurred in colder climates was affected by the new ambient temperature, but as evolution occurred in the population, these behavioural and physiological effects were no longer dependent on external cues for their expression. After using their adaptability to respond to the new environmental conditions, the house finch populations spontaneously expressed the characteristics that best fitted them to their new habitats.11

The adaptable house finch. Photo by Thomas Quine (2007), Wikipedia, https://commons.wikimedia.org/​wiki/​File:Male_House_Finch_profile_(23910087075).jpg. CC BY 2.0.

Conclusions

35Adaptability probably appeared at an early stage in biological evolution. Its role in promoting evolutionary change has not been much investigated. Even so it is plausible that, like the other ways in which an organism’s activities can affect its descendants, adaptability has been important. Adaptability can accelerate the rate at which challenges set by the environment can be met. The effect of plasticity on evolution may have become increasingly powerful as animals, in particular, became more complex. Elements could be recombined in different ways to perform different functions. This evolutionary process could lead to the establishment of increasingly elaborate organization and patterns of behaviour.

36Darwin’s famous metaphor of natural selection is deeply embedded in the modern language of biologists. Natural selection is treated as an agent in much the same way as humans are agents in artificial selection. The strictures on the misuse of the selection metaphor in evolutionary biology will not change many minds since it is not easy to give up the habits of a lifetime. Hopefully, though, the more adventurous will try replacing ‘selection’ in their writing with ‘Darwinian evolution’. This would gives honour where it is due and encourage the view that behaviour does play an active role in evolution.

37With the growing acceptance that organisms are not passive in relation to their role in the evolution of their descendants, focus on the adaptability driver helps to bring together studies of development with those of evolution, a principal aim of this book. By doing so, the systems approach provides satisfying explanations for the appearance of design in so much behaviour.

Notes

1 The mantra among most evolutionary biologists used to be that evolution involves changes in the frequencies of genes. By contrast Waddington argued that Darwinian evolution acts on the outcomes of development (Waddington, C.H. (1975), The Evolution of an Evolutionist. Ithaca, NY: Cornell University Press). In other words evolution involves changes in phenotypes.

2 Gluckman, P.D., Hanson, M.A. & Buklijas, T. (2010), A conceptual framework for the developmental origins of health and disease. J. Devel. Origins Health Disease 1.01, 6–18, https://doi.org/10.1017/s2040174409990171

3 Chali, D., Enquselassie F. & Gesese M. (1998), A case-control study on determinants of rickets. Ethiop. Med. J. 36.4, 227–234

4 Bateson, P., Gluckman, P. & Hanson, M., The biology of developmental plasticity and the Predictive Adaptive Response hypothesis. J. Physiol. 592.11, 2357–2368, https://doi.org/10.1113/jphysiol.2014.271460

5 Braun, E. & David, L. (2011), The role of cellular plasticity in the evolution of regulatory novelty. In: Gissis, S. B. & Jablonka, E. (eds.), Transformations of Lamarckism: From Subtle Fluids to Molecular Biology. Cambridge, MA: MIT Press, pp. 181–191.

6 The importance of the active role of behaviour in evolution is discussed in Bateson, P. (2013), New thinking about biological evolution. Biol. J. Linn. Soc. 112.2, 268–275, https://doi.org/10.1111/bij.12125

7 Michel, A.P. (2010), Widespread genomic divergence during sympatric speciation. PNAS 107.21, 9724–9729, https://doi.org/10.1073/pnas.1000939107

8 Humphrey, N. (1986), The Inner Eye. London: Faber & Faber.

9 Foster, S.A. et al. (2015), Evolutionary influences of plastic behavioral responses upon environmental challenges in an adaptive radiation. Integr. Comp. Biol. 55.3, 406–417, https://doi.org/10.1093/icb/icv083

10 Beall, C.M. (2007), Two routes to functional adaptation: Tibetan and Andean high-altitude natives. PNAS 104.1, 8655–8660, https://doi.org/10.1073/pnas.0701985104

11 Badyaev, A.V. (2009), Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Phil. Trans. Roy. Soc. B, 364.1520, 1125–1141, https://doi.org/10.1098/rstb.2008.0285

Table des illustrations

Légende Nick Humphrey. Photo by LittleHow (2010), Wikipedia, https://commons.wikimedia.org/​wiki/​File:Nick_Humphrey.jpg, CC BY-SA 3.0.
URL http://books.openedition.org/obp/docannexe/image/3894/img-1.jpg
Fichier image/jpeg, 16k
Légende The adaptable house finch. Photo by Thomas Quine (2007), Wikipedia, https://commons.wikimedia.org/​wiki/​File:Male_House_Finch_profile_(23910087075).jpg. CC BY 2.0.
URL http://books.openedition.org/obp/docannexe/image/3894/img-2.jpg
Fichier image/jpeg, 22k

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