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Behaviour, Development and Evolution

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Patrick Bateson

8. Genes in Development and Evolution

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  • 1 This debate is well-described in Noble, D. (2016), Dance to the Tune of Life: Biological Relativity(...)
  • 2 See Sultan, S. (2015), Organism and Environment: Ecological Development, Niche Construction, and Ad (...)

1For the Darwinian evolutionary mechanism to work, something must be inherited with fidelity. Even if a single change in DNA provides the basis for a distinctive beneficial character of an individual, that is not sufficient for the development of the character. This gets to the heart of a lively debate in biology.1 Genes have been defined in many different ways: as units of physiological function, units of recombination, units of mutation, or units of evolutionary process — when they have sometimes been imbued with ‘selfish’ intentions in order to help the understanding of the complexities of evolution. The problem of definition has been made worse as it has become clear that the same molecule of DNA may serve in processes that differ in function. In the post-genomic era, the emerging concepts of the gene pose a significant challenge to conventional assumptions about the relationship between genome structure and function, and between genotype and developed characteristics.2

  • 3 Keller, E.F. (2000), Century of the Gene. Cambridge, MA: Harvard University Press. An accessible an (...)

2The word ‘gene’ does not, then, have a clear unambiguous meaning.3 For some scientists it meant simply a sequence of DNA, for others it referred specifically to those segments of DNA that are transcribed into ribonucleic acid (RNA) and then translated into a protein. By contrast, many segments of RNA — the so-called non-coding RNAs — have regulatory functions, and the term ‘gene’ is extended by many molecular geneticists to include the DNA sequences coding for these RNAs. These different meanings of gene sometimes get conflated, with subsequent confusion of thought.

  • 4 Many of the DNA strands come in many different forms that provide the basis for forensic studies an (...)

3Despise the semantic confusion, the use of variations in DNA to identify individuals is crucially important in the forensic analysis of crimes. In other areas of biology the variation is used to establish relationships between species and the probable evolution of taxonomic groups. Moreover the technologies for producing new types of crops that are resistant to disease or water shortage are now well developed. Scientists collaborating on the Human Genome Project have elucidated nearly all the DNA sequences on all 23 pairs of chromosomes found in a human cell.4 It is a staggering achievement. Much epidemiological research in recent years has been based on sequencing the entire human genome and looking at mutant alleles that correlate with disease. A surprising result of these genomewide association studies has been that, even when large populations are studied, and the disease of interest is common, such as Type 1 diabetes, few significant genetic effects are found and the effects of any one specific difference in DNA are generally small. Single-gene effects are unusual and largely restricted to relatively rare diseases, such as phenylketonuria or haemophilia. The excitement about what is being done should be greatly moderated. ‘The Book of Life’, as one leading scientist called it, does not provide the complete story about human nature.

Genes in development

  • 5 The use of the term information exclusively applied to genes has been sharply criticised by Oyams, (...)

4The starting points of development include the genome which provides information of a kind.5 They also include factors external to the genome; the social and ecological conditions in which the individual grows up are crucial. A low-tech cooking metaphor serves to shift the focus onto the multi-causal and conditional nature of development. Using butter instead of margarine may make a cake taste differently when all the other ingredients and cooking methods remain unchanged. But if other combinations of ingredients or other cooking methods are used, the distinctive difference between a cake made with butter and a cake made with margarine may vanish. Similarly, a baked cake cannot readily be disaggregated into its original raw ingredients and the various cooking processes, any more than a behaviour pattern or a psychological characteristic can be disaggregated into its genetic and environmental influences and the developmental processes that gave rise to it. In the cooking analogy, the raw ingredients represent the many genetic and environmental influences, while cooking represents the biological and psychological processes of development. Nobody expects to find all the separate ingredients represented as discrete, identifiable components in a cake. Similarly, nobody should expect to find a simple correspondence between a particular gene (or a particular experience) and particular aspects of an individual’s behaviour or personality.

The process of making a cake. Photo by Roozitaa (2012), Wikimedia, https://commons.wikimedia.org/​wiki/​File:Making_Chiffon_cake_2.jpg, CCBY3.0.

5The language of a gene ‘for’ a particular characteristic is exceedingly muddling to the non-scientist — and, if the truth be told, to some scientists as well. What the scientists mean (or should mean) is that a genetic difference between two groups is associated with a difference in a characteristic. They know perfectly well that other things are important and that, even in constant environmental conditions, the outcome depends on a combination of many genes. Particular combinations of genes have particular effects, and a gene that fits into one combination may not fit into another. Unfortunately, the language of a gene ‘for’ a characteristic has a way of sometimes seducing scientists themselves into believing their own sound-bites. Such language rests on a profound misunderstanding.

6The notion that genes are simply blueprints for an individual human is hopelessly misleading. In a blueprint, the mapping works both ways: starting from a finished house, a room can be found on the blueprint, just as the room’s position is determined by the blueprint during the building process. This straightforward mapping is not true for genes and individual human behaviour patterns, in either direction.

7The common image of a genetic blueprint for behaviour fails because it is too static, suggesting that adult organisms are merely expanded versions of the fertilized egg. In reality, developing organisms are dynamic systems that play an active role in their own development. Even when a particular base in a strand of DNA or a particular experience is known to have a powerful negative effect on the development of behaviour, biology has an uncanny way of finding alternative routes. If the normal developmental pathway to a particular form of adult behaviour is impassable, another way may often be found. The individual may be able, through its behaviour, to match its environment to suit its own characteristics.

8Strands of DNA do not, on their own, make behaviour patterns or physical attributes. They code for polypeptides, the precursors of proteins or small molecules of RNA. The proteins are crucial collectively to the functioning of each cell in the body. Some proteins are enzymes, controlling biochemical reactions, while others form the physical structures of the cell. These protein products of genes do not work in isolation, but in a cellular environment created by local conditions.

9The DNA content of an individual organism can be measured accurately. When the amount of DNA is compared to the relative size of the nervous system and the complexity of behaviour it generates, a lack of correlation is surprising. Mice have 6000 times as much DNA as bacteria which makes sense if the differences in the DNA are responsible for the differences in complexity. Humans have no more DNA than mice. In other words, whatever else happened in evolution, the gradual emergence of behavioural complexity within the mammals was not achieved by accumulating the genes that code for protein components. Some of the lack of association may be explained by the number of genes not being the same as the amount of DNA. It may also be attributed to ‘junk’ DNA which, it used to be supposed, had no effect on the organism’s developed characteristics. The discovery that some or all genes in this so-called junk code for small molecules of RNA has profound implications for the regulation of development. At the very least, it means that the growth of nervous systems and the emergence of behaviour are critically dependent on regulation and the combinatorial action of genes. This means that the correspondence between genes and behaviour is never likely to be simple. Many genes really do code for polypeptides, of course, but they represent nothing else since the process of development is generative. A small subset of genes and cytoplasmic conditions start the whole process after fertilisation of the egg. These starting conditions create products that switch off some active genes, switch on others and bring the developing components into contact with new influences from outside. And so the whole process continues until death.

10It is clear, then, that because of the system in which they are embedded, no simple correspondence is found between individual genes and particular behaviour patterns or psychological characteristics. Genes do not code for parts of the nervous system and they certainly do not code for particular behaviour patterns. Any one aspect of behaviour is influenced by many genes, each of which may have a big or a small effect. Conversely, changes in any one of many genes can have a major disruptive effect on a particular aspect of behaviour. A disconnected wire can cause a car to break down, but this does not mean that the wire by itself is responsible for making the car move.

11Without a strong set of binding ideas, it isn’t easy to think about all aspects of the various strands of evidence, which often seem to point in opposite directions. Some theorists have argued that the seemingly simple and orderly characteristics of development (such as they are) are generated by dynamic processes of great complexity. Many mathematical techniques, such as catastrophe theory and ‘chaos’, have been developed to deal analytically with the complexities of dynamical systems. A promising empirical approach is collecting evidence across different levels of analysis.

Heritability

12When offspring look like their parents or other members of their family, it is reasonable to assume that they have inherited something. The total set of characteristics that are inherited are rarely correlated. So in human families a boy might have the big nose of his uncle, the ginger hair of his father and the retiring disposition of his grandmother. Mendelian inheritance and the recombination of characteristics in each generation explains why this should be so. Also, many different processes might be involved; most are genetic but some are environmental. Attempts to sort out the different possibilities have risen to the concept of heritability. Instead of asking whether a child’s characteristics are caused by genes or caused by the environment, the question instead became: ‘How much is due to each?’ In a more refined form, the question is posed thus: ‘How much of the variation between individuals in a given character is due to differences in their genes, and how much is due to differences in their environments?’

13The meaning of heritability is best illustrated with an uncontroversial characteristic such as height, which is clearly influenced by both the individual’s family background (genetic influences) and nutrition (environmental influences). The variation between individuals in height attributable to variation in their genes may be expressed as a proportion of the total variation within the population sampled. This index is known as the heritability ratio. The higher the figure, which can vary between 0 and 1.0, the greater the contribution of genetic variation to individual variation in that characteristic. So, if people differed in height solely because they differed in their genes, the heritability of height would be 1.0; if, on the other hand, variation in height arose entirely from individual differences in environmental factors such as nutrition then the heritability would be zero.

14Calculating a single number to describe the relative contribution of genes and environment has obvious attractions. Estimates of heritability are of undoubted value to animal breeders, for example. Given a standard set of environmental conditions, the genetic strain to which a pig belongs will predict its adult body size better than other variables such as the number of piglets in a sow’s litter. If the animal in question is a cow and the breeder is interested in maximising its milk yield, then knowing that milk yield is highly heritable in a particular strain of cows reared under standard rearing conditions is important.

15Behind the deceptively plausible ratios lurk some fundamental problems. For a start, the heritability of any given characteristic is not a fixed and absolute quantity — tempted though many scientists have believed otherwise. Its value depends on a number of variable factors, such as the particular population of individuals that has been sampled. For instance, if heights are measured only among people from affluent backgrounds, then the total variation in height will be much smaller than if the sample also includes people who are small because they have been undernourished. The heritability of height will consequently be larger in a population of exclusively well-nourished people than it would be among people drawn from a wider range of environments. Conversely, if the heritability of height is based on a population with relatively similar genotypes — say, native Icelanders — then the figure will be lower than if the population is genetically more heterogeneous; for example, if it includes both Icelanders and African Pygmies. Thus, attempts to measure the relative contributions of genes and environment to a particular characteristic are highly dependent on who has been measured and in what conditions.

16Another problem with heritability estimates is that they reveal nothing about the ways in which genes and environment contribute to the biological and psychological processes of development. This point becomes obvious when considering the heritability of a characteristic such as ‘walking on two legs’. Humans walk on fewer than two legs only as a result of environmental influences such as war wounds, car accidents, disease or exposure to toxins before birth. In other words, all the variation within the human population results from environmental influences, and consequently the heritability of ‘walking on two legs’ is zero. And yet walking on two legs is clearly a fundamental property of being human, and is one of the more obvious biological differences between humans and other great apes such as chimpanzees or gorillas.

17It obviously depends heavily on genes, despite having a heritability of zero in humans. A low heritability clearly does not mean that development is unaffected by genes.

18The effects of a particular set of genes depend critically on the environment in which they are expressed, while the effects of a particular sort of environment depend on the individual’s genes. Even in animal breeding programmes that use heritability estimates to practical advantage, care is still needed. If breeders wish to export a particular genetic strain of cows that yields a lot of milk, they would be wise to check that the strain will continue to give high milk yields under the different environmental conditions of another country.

Epigenetics

  • 6 See Spector, T. (2012), Identically Different: Why You Can Change Your Genes. London: Weidenfeld & (...)

19The often uncanny similarities between identical twins provide striking evidence for the importance of genes in shaping physical and behavioural characteristics. On the other hand identical twins can differ markedly from each other.6 The cues that come from the environment are often those that regulate the regulators. Much of the plasticity seen in development is generated this way. The course of an individual’s development may be radically different depending on the nature of these cues. Individuals with identical genomes do not necessarily have identical adult characteristics. In the case of schizophrenia for instance one identical twin may develop the disease while the other does not.

  • 7 Shields, J. (1962), Monozygotic Twins Brought up Apart and Brought up Together. Oxford: Oxford Univ (...)

20Identical twins reared apart are sometimes more like each other than those reared together.7 To put it another way, rearing two genetically identical individuals in the same environment can make them less similar. This fact pleases neither the extreme environmental determinist nor the extreme genetic determinist. The environmental determinist supposes that twins reared apart must have different experiences and should therefore be more dissimilar in their behaviour than twins who grow up together in the same environment. The genetic determinist does not expect to find any behavioural differences between genetically identical twins reared together; if they have had the same genes and the same environment, then how can they be different? Of course, one twin provides a social environment for the other and often one sibling will not do what the other one is doing.

  • 8 The developmental processes involved were subsumed under the general heading of ‘epigenetics’ by Wa (...)

21All processes involved in development have been subsumed under the heading of epigenetics. In a restricted sense, epigenetic processes are those that result in the silencing or activation of gene expression through such modification of the roles of DNA or its associated RNA and protein. The term has therefore come to describe, for many, those molecular mechanisms through which both dynamic and stable changes in gene expression are achieved, and ultimately how variations in extracellular input and experience by the whole organism of its environment can modify regulation of DNA expression. Some authors continue to use this broader definition of epigenetics to describe all the developmental processes, behavioural and physiological as well as molecular, that bear on the character of the organism.8 In all these usages, epigenetics usually refers to what happens within an individual developing organism. Whether a broad or restricted view of epigenetics is taken, the discovery of epigenetic phenomena has led to a revolution in thinking about the importance of developmental processes.

22The molecular processes involved in the development of an organisms characteristics were initially worked out for the regulation of cellular and proliferation. All cells within the body contain the same genetic sequence information, yet each lineage has undergone specialisation to become a skin cell, hair cell, heart cell, and so forth. These differences within a developing individual are inherited from mother cells to daughter cells. The process of differentiation involves the expression of particular genes for each cell type in response to cues from neighbouring cells and the extracellular environment, with the silencing of others. Genes that have been silenced at an earlier stage remain silent after each cell division (except in cancers). Such gene silencing provides each cell lineage with its characteristic pattern of gene expression. These epigenetic marks are faithfully duplicated across each cell division, stable cell differentiation results and serves many different functions.

23Molecular mechanisms are involved in the activation or silencing of genes. One of the silencing mechanisms involves a process known as methylation. Chromosomes consist of strands of chromatin. DNA is organized along chromatin in packets known as nucleosomes. These have a molecule with a hydrogen atom on one of its arms. If this is replaced by a methyl group, the nucleosomes close up and the DNA is less able to be expressed as messenger RNA which in turn forms the template for synthesising protein. Conversely if the methyl group is replaced by a hydrogen atom, the DNA on the affected nucleosomes can be expressed.

24An important mechanism in development involves small molecules of non-coding micro-RNA. When these small molecules are expressed they may bind onto messenger RNA which links as an intermediate between DNA and protein, with the result that the gene that expressed the messenger RNA loses its capacity to code for protein and is effectively silenced. The regulators have themselves to be regulated, and unraveling the networks will take a great deal of research, but the general principles involved in producing differences in cell lines are already apparent.

  • 9 Rowell, C.H.F. (1971), The variable coloration of the acridoid grasshoppers. Adv. Insect Physiol. 8 (...)

25Many examples in biology demonstrate the dependence of gene expression on local conditions. After a fire on the high grassland planes of East Africa, for example, the young 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, and 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.9 If the young grasshoppers are placed on black paper they become black when they moult to the next stage. But if they are placed on pale paper the moulting grasshoppers are the normal green colour. The grasshoppers actively select habitats with the colour 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 once they reach adulthood they are committed to one colour. This striking example illustrates at the level of the whole organism the role of epigenetics in development.

Selfish genes

  • 10 Dawkins, R. (1976), The Selfish Gene. Oxford: Oxford University Press.

26Turning to evolutionary processes, a crucial question is at what level of organisation does the process of Darwinian evolution act? The selfish gene approach made famous by Richard Dawkins10 has been valuable in helping to understand self-sacrifice, and conflicts between the sexes and generations. The language of genes having metaphorical intentions helps people to deal with the complicated dynamics of evolution. Such explanations are not meant to be treated in the way usually employed by an experimental scientist; they provide a framework in which to think about phenomena that would otherwise be neglected.

27Most people get their minds around complex processes when they attribute intentions to them. It is a powerful way of thinking about systems. Weather forecasters, having to cope with explaining appallingly complex problems, make statements like: ‘The depression is trying to move in from the west’. The language encourages thought about endpoints rather than with all the details of how they are achieved.

Richard Dawkins author of The Selfish Gene. Photo by Marty Stone (2009), Wikimedia, https://commons.wikimedia.org/​wiki/​File:Richard_Dawkins_35th_American_Atheists_Convention.jpg, CC BY 2.0.

28Is the gene the target of selection in evolution? It may be helpful to forget biology for a moment and think about the spread of a new brand of biscuit in supermarkets. Consider the spread from the perspective of the recipe. While shoppers select biscuits and eat them, it is the recipe for making desirable biscuits that survives and spreads in the long run. A phrase in the recipe might specify the amount of sugar to be added and makes the difference between a popular and a less popular biscuit. In that sense it is selfish. This novel way of looking at things is unlikely to mislead anyone into believing that what shoppers really do in supermarkets, when they pick a particular brand of biscuit off the shelves, is select a word in the recipe used for making the biscuits. They select the brand of biscuit they like.

29Darwin used his metaphor of ‘natural selection’ because he was impressed by the ways in which plant and animal breeders artificially selected the characters they sought to perpetuate. The agents of differential survival and differential reproductive success will usually be characteristics of whole individuals including the structures they make, but they might be characteristics of molecules or of symbiotic groups, or the evolvability of taxonomic lineages.

30The power of the selfish gene language has been used misleadingly to prop up the idea of the gene as ‘programmer’. The mechanistic language does not translate into the teleological language. For population geneticists, a genetic difference is identified by means of a biochemical, physiological, structural or behavioural difference between organisms (after other potential sources of difference have been excluded by appropriate procedures). The popular language of genes’ intentions and the more orthodox language of genetic differences are not simply alternative ways of describing the same thing. In the technically precise language of population geneticists, a genetic allele must be compared with another from which it differs in its consequences. In selfish-gene language, it stands alone as an entity, absolute in its own right. The perception generated by one meaning of gene does not relate to the same evidence as that generated by the other.

Conclusions

31An important point, often made but equally often ignored, is that correlations between the behaviour patterns of the parent and those of the do not necessarily arise because they have genes in common. They may arise because other conditions that are necessary for the peculiarities of their behaviour are shared. Common odours and preferences for familiar smells might arise from the particular combination of bacteria that breakdown the fats secreted onto the body surface. When the bacteria pass from mother to offspring, so does the source of her special smell. This is not to downplay the roles of genes. But it emphasises that the nothing-but approach to genes is clearly wrong. Taking a systems approach to the role of genes generates much more fruitful understanding than treating them as providing single causes for development and evolution.

Notes

1 This debate is well-described in Noble, D. (2016), Dance to the Tune of Life: Biological Relativity. Cambridge: Cambridge University Press. Denis Noble argues that living organisms operate at multiple levels of complexity and must therefore be analysed from a multi-scale, relativistic perspective. Noble explains that all biological processes operate by means of molecular, cellular and organismal networks. The interactive nature of these fundamental processes is at the core of biological relativity and, as such, challenges simplified molecular reductionism. Noble shows that such an integrative view emerges as the necessary consequence of the rigorous application of mathematics to biology. Drawing on his pioneering work in the mathematical physics of biology, he shows that what emerges is a deeply humane picture of the role of the organism in constraining its chemistry, including its genes, to serve the organism as a whole, especially in the interaction with its social environment. This humanistic, holistic approach challenges the common gene-centred view held by many in modern biology.

2 See Sultan, S. (2015), Organism and Environment: Ecological Development, Niche Construction, and Adaptation. Oxford: Oxford University Press, https://doi.org/10.1093/acprof:oso/9780199587070.001.0001

3 Keller, E.F. (2000), Century of the Gene. Cambridge, MA: Harvard University Press. An accessible and clear-headed introduction to genetics is given in Griffiths, P. & Stotz, K. (2013), Genetcs and Philosophy: An Introduction. Cambridge: Cambridge University Press.

4 Many of the DNA strands come in many different forms that provide the basis for forensic studies and attempts to discover genetic relationships between people.

5 The use of the term information exclusively applied to genes has been sharply criticised by Oyams, S. & Lewontin, R. (2000), The Ontogeny of Information. 2nd ed. Durham, NC: Duke University Press, https://doi.org/10.1215/9780822380665. As the title of her book suggests, all factors impinging on the developing organism provide information of a kind.

6 See Spector, T. (2012), Identically Different: Why You Can Change Your Genes. London: Weidenfeld & Nicolson.

7 Shields, J. (1962), Monozygotic Twins Brought up Apart and Brought up Together. Oxford: Oxford University Press.

8 The developmental processes involved were subsumed under the general heading of ‘epigenetics’ by Waddington, C.H. (1957) in The Strategy of the Genes (London: Allen & Unwin). He distinguished this term from the eighteenth-century term ‘epigenesis’, which had been used to oppose the notion that all the characteristics of the adult were preformed in the embryo. More recently, epigenetics has become mechanistically defined as the molecular processes by which traits defined by a given profile of gene expression can persist across mitotic cell divisions, but which do not involve changes in the nucleotide sequence of the DNA (see Carey, N. (2012). The Epigenetics Revolution: How Modern Biology is Rewriting Our Understanding of Genetics, Disease and Inheritance. London: Icon Books Ltd.). The general principles apply at higher levels of organisation and are involved in mediating many aspects of developmental plasticity seen in intact organisms. For that reason, some authors continue to use Waddington’s broader definition of epigenetics to describe all the developmental processes that bear on the character of the organism. The processes involved in gene expression and suppression can be transmitted from one generation to the next (See Gissis, S.B. & Jablonka, E. (2011), Transformations of Lamarckism: From Subtle Fluids to Molecular Biology. Cambridge, MA: MIT Press, and Miska, E. A. & Ferguson-Smith, A. C. (2016), Transgenerational inheritance: models and mechanisms of non-DNA sequencebased inheritance, Science 354.6308, 59–63, https://doi.org/10.1126/science.aaf4945). Further support for the revision of the orthodoxies of evolutionary theory has come from microbiology (Shapiro, J. (2011), Evolution: A View from the 21st Century. Upper Saddle River, NJ: FT Press Science). Shapiro argues that cells must be viewed as complex systems that control their own growth, reproduction and shape their own evolution over time. He referred to it as a ‘systems engineering’ perspective and noted interestingly that, ‘Most of the interactions between biomolecules tend to be relatively weak and need multiple synergistic attachments to produce stable functional complexes’ (Shapiro, 2011: 31).

9 Rowell, C.H.F. (1971), The variable coloration of the acridoid grasshoppers. Adv. Insect Physiol. 8, 145–198, https://doi.org/10.1016/s0065-2806(08)60197-6

10 Dawkins, R. (1976), The Selfish Gene. Oxford: Oxford University Press.

Table des illustrations

Légende The process of making a cake. Photo by Roozitaa (2012), Wikimedia, https://commons.wikimedia.org/​wiki/​File:Making_Chiffon_cake_2.jpg, CCBY3.0.
URL http://books.openedition.org/obp/docannexe/image/3892/img-1.jpg
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Légende Richard Dawkins author of The Selfish Gene. Photo by Marty Stone (2009), Wikimedia, https://commons.wikimedia.org/​wiki/​File:Richard_Dawkins_35th_American_Atheists_Convention.jpg, CC BY 2.0.
URL http://books.openedition.org/obp/docannexe/image/3892/img-2.jpg
Fichier image/jpeg, 22k