On the Place of the Individual in Evolution

1. Introduction

Charles Darwin (1809-1882) described the process of evolution as 'descent with modification' (Darwin, 1859). He had in mind the way in which organic forms can change within an evolutionary lineage over numerous generations. With each generation, offspring, although resembling their parents are, nevertheless, slightly different from them. If heritable, these differences could become more widespread within a population. Furthermore, certain features could even become exaggerated over time to the extent that descendents became increasingly unlike their more distant ancestors. However, these modifications had first to pass through the filter of natural selection. Advantageous variations would tend to persist; disadvantageous variations would tend to be lost. Darwin was particularly concerned to point out that this process formed a basis for speciation. The division into species, in Darwin's day, was largely based upon naked eye assessments of form.

The focus of Victorian naturalists was quite unlike that of modern biologists. Their focus was upon the organism. These they collected and categorised. It was outward appearance that formed the basis for the classification of species. Significantly, the idea of 'type specimens' developed. It was against these that newly discovered forms would be compared to see if they might be of the same or perhaps a new species. The emphasis was, therefore, very much upon visual comparison. However, visual similarities can be deceptive. The process of evolution can act in a convergent manner. Ancestrally different organisms can take on quite similar outward appearances; they can converge on a similar physical form by way of a solution to a particular environmental or selective pressure. As new techniques became available, a greater range of distinguishing features have come to be drawn upon when trying to ascertain the species to which an organism belongs. Since the era of the Victorian naturalist, there has been a shift away from the level of the organism as an individual and from its outward appearance towards ever finer levels of discrimination made within. Yet, it should never be overlooked that it was from what was observed at the level of the individual organism that the theory of evolution was originally derived.

2. Shifting Focus – Genes and Populations

Since Darwin's time the focus of attention has shifted somewhat. The organism is no longer the prime focus of attention in evolutionary biology. Sometimes it even seems to be overlooked as attention has come to be somewhat bifurcated into the study of molecular level genetics and population level genetics. Given this shift of attention, it is important not to lose sight of the organism as an individual entity. Not to do so could mean that many of the useful ideas and ways of thinking that were evident in the past are missed. It is always interesting and sometimes helpful to pause and look to the whole organism and its place in the wider biological scheme of things. That organism is the individual mentioned in the title of this chapter. Although plants may be considered to exist as individuals, the main focus here will be upon individual animal organisms. There is a certain entirety about such individuals which is both different to the sum of its component parts and different to its aggregation into groups. Component parts and aggregations each behave in ways quite dissimilar to the ways in which individuals behave.

Of the changes in scientific outlook that have taken place in the century and a half since the publication of Darwin's 'On the Origin of Species' – the book that launched modern evolutionary biology – two are of particular interest here. Firstly, the purview of many parts of biological science – including evolutionary biology – has become ever more reductionist. Secondly, particular attention has come to be paid to group dynamics and to phenomena that arise out of aggregating individuals.

There are two subtly different strands to reductionism. One is the approach of trying to understand complex objects, such as organisms, in ever finer physical detail. It seeks to understand an object in terms of the interactions between its component parts. However, reductionism can also be an essentially philosophical position. This holds that complex objects, such as organisms, are nothing more than just the sum of their component parts. That being the case, to understand the whole, all that one need do is understand the workings of the components. While one is a methodological approach and the other an intellectual one, it is easy for the two to overlap and even to become entwined. It is very easy to slip from a methodological reductionism – perfectly appropriate for one's practical work – into a philosophical reductionism which assumes that explanations for higher level phenomena can be found in terms of the operation of the smaller scale phenomena upon which one is working. In one of its most extreme forms – genetic determinism – philosophical reductionism holds that all phenomena expressed at the level of the organism can be explained in purely genetic terms (Dawkins, 1976). For some this also includes the behaviours displayed by organisms. The explanation of behaviour in genetic terms has long been a contentious issue (see for example, Rose & Rose, 2001). With the emergence of systems biology (Boogerd et al., 2007; Kitano, 2002), the organism need no longer be seen as something containing myriads of simplistic cause-and-effect connections with genes as the prime movers but as a network of effects which combine in complex and unpredictable ways. The organism is now beginning to be seen more as a system; a network of inter-related events. While the tendency towards reductionism is open to future modification, the tendency towards aggregating individuals is currently less open to change. Alternative approaches have yet to emerge.

Following the publication of 'On the Origin of Species', Darwin's ideas immediately proved both popular and controversial. However, while there was intuitive sense in what Darwin described, the processes involved in bringing about 'descent with modification' were less obvious. For the evolution of organisms by natural selection to occur, certain conditions were necessary. Of fundamental importance, was the need for a means of reproduction. Animals, for example, must be able to produce offspring. These offspring, while resembling their parents, should not be identical to them. Offspring should have scope to differ from their parents or else there would be no modification. Some of these variations would prove advantageous to the offspring who would then fare better than other members of their species. They would tend to produce more offspring of their own and their characteristics would become more numerous. Some variations would prove disadvantageous to these offspring who would fare less well. Those disadvantaged in this way would leave fewer or no offspring. Some might even perish as a result of their disadvantageous variations before even attempting to reproduce. Offspring with these characteristics would become less numerous. However, in the late nineteenth century, it was not known how these variations came about nor how they might be transmitted from generation to generation. It was clear that the offspring of plants and animals were like their parents and that they inherited characteristics from them albeit with minor variations but exactly how was not known. Without this knowledge, further scientific development of the theory of evolution was restricted. What ideas there were about mechanisms of inheritance were at odds with the notion of evolution. It was only at the turn of the twentieth century that a solution to this problem began to emerge.

3. The Century of the Gene

In biology, the twentieth century is likely to be remembered as the century of the gene. In particular, the concept of the gene came to dominate the second half of that century with it coming to appear regularly in the non-scientific media. Few non-scientific members of the general public have not heard of 'the gene'. The second half of the twentieth century is associated firstly with the discovery of the structure of the DNA molecule upon which heritable information is stored (Watson & Crick, 1953). Then, latterly, at the close of the century, the Human Genome Project succeeded in mapping the human genetic code with the much heralded promise that significant health benefits would follow. So far, these benefits have largely failed to appear.

However, the century of the gene began more quietly with the rediscovery of Mendel's laws of inheritance and his work originally published in 1866. Mendel's work had been largely overlooked in the intervening years. Few had ever made reference to it in their own work. When first published, Mendel's work had been seen as being more about hybridization in plants than about mechanisms of inheritance that might apply to all organisms. By the end of the nineteenth century, attention was beginning to be applied to finding an explanation for discontinuous characteristics of inheritance; something that the prevailing notion of blending inheritance, as it was called, could not explain. Previously, it had been assumed that inheritance involved a process of blending the characteristics of both parents. However, this was problematic. Had this been the case, it would have led to a mere averaging out of characteristics over the space of relatively few generations. Inherited characteristics clearly did not behave in that way - least of all the differentiation into male and female. These qualities clearly never blended. Neither could blending inheritance explain the emergence of new characteristics within an evolutionary lineage. However, Mendel had shown inheritance to be particulate in nature. Particulate inheritance – the inheritance of discrete packets of information about phenotypic characteristics which were also open to subtle internal variation – could explain how characteristics changed between generations in a variety of ways. It could explain what blending inheritance could not. Furthermore, by extension, it could also explain aspects of the process of evolution.

Three workers have been variously credited with the rediscovery of Mendel's laws of inheritance: Carl Correns (1864-1933), Erich von Tschermak (1871-1962) and Hugo de Vries (1848-1935). (It should be noted that there is some debate among historians of science over the relative roles played by each in this rediscovery (Henig, 2009).) Significantly, Correns (1900) cited both Darwin and Mendel in his work and so might be said to be the first to bridge both the theories of inheritance and evolution. However, Correns does not appear to have fully appreciated the relevance of the theory of inheritance to the theory of evolution. This was to occur in stages during the first half of the twentieth century when the modern evolutionary synthesis became established. This synthesis was a combination of findings from a range of different areas within biology. Central to this was a combining of natural selection and Mendelian genetics. This led to a revival of interest in evolutionary biology which had gone through a somewhat quiescent phase following its initial successes. In 1930, in his 'The Genetical Theory of Natural Selection', R.A. Fisher (1890-1962) was able to show that Mendelian genetics and evolution by natural selection were consistent with each other (Fisher, 1930).

As well as a mechanism for inheritance, it was necessary for the effects of inheritance to be understood at a population level. Out of this, the science of population genetics arose. The changes that occur in gene frequencies over time came to be seen as that which really evolves. Previously, in the nineteenth century, it was form that had been the focus of attention. Evolution was characterised by a modification of form and appearance over time. However, modern evolutionary biology now gives particular emphasis to the behaviour of gene frequencies in population terms. It is how gene frequencies within populations change over time which demonstrates how the process of evolution is occurring. That being the case, individual organisms have come to be seen in a somewhat different way. They are the products of a population's gene pool. Thus, the individual organism may be described as an evolved rather than an evolving entity. Although it must change throughout its life as it grows and develops, the individual organism is little more than a node on the timeline of a species' evolutionary history. It is typically seen as a transient repository of genes which were obtained as copies from its parents; copies which are waiting to be passed on, as further copies, to the next generation of offspring. The individual is but the offspring of the preceding generation and the progenitor of the next. Thus, the individual organism is often seen as being of secondary importance in modern evolutionary biology. For many, it is simply how gene frequencies behave that really matters.

4. Stochastic Effects

A key figure in the modern evolutionary synthesis was the American geneticist Sewall Wright (1889-1988). Wright recognised how genes could act together in combinations or complexes. While much of the mathematical description of population genetics is, for theoretical purposes, based on large (sometimes infinitely large) populations, Wright recognised how relatively small geographically isolated populations could exhibit a process he called 'genetic drift' (Wright, 1929). This was a change in the gene frequency within a population brought about by random effects and not by natural selection per se.

The relative importance of genetic drift versus natural selection as the drivers of evolutionary change within a species has been debated at intervals since Wright first made this realisation. Fisher, for example, thought that genetic drift played a relatively minor role in evolution. This opinion came to be the orthodox view during the middle of the twentieth century. However, in 1968, Motoo Kimura (1924-1994) proposed the neutral theory of molecular evolution (Kimura, 1968). This revived the debate about the relative importance of genetic drift. The neutral theory of molecular evolution proposes that most of the evolutionary changes at molecular level were caused by a random drift in mutations in the genetic material and were selectively neutral. Kimura was not proposing an alternative to evolution by natural selection. He saw the two as consistent with each other. However, he sought to apportion a greater role for genetic drift than had previously been accepted.

Whatever the precise relative merits of these two mechanisms, it is clear that the effect of genetic drift is greater the smaller the population concerned. Where populations are small, stochastic effects are more noticeable than in large populations. In large populations, chance events can be masked or subsumed by the numbers involved. This is particularly significant in relation to two important population reducing phenomena:

· Population (or Genetic) Bottleneck

· The Founder Effect

Population (or genetic) bottlenecks occur when there is a significant reduction in population size – or where a significant proportion of a population is prevented from breeding in some way. This reduces the size of the gene pool from which the genes to be conveyed into the next generation can be drawn. The founder effect is similar but instead of a reduction in the size of the whole population, a small sub-group drawn from within a parent population becomes separated from it. This may occur, for example, as a result of migration. From this subgroup, a new geographically distinct population may arise. In both examples, the genetic diversity within the parent population is no longer represented in the smaller group. Accordingly, the range of heritable characteristics will not be the same as was the case for the full population; only a random sample drawn from that population will be available. Within such a sample, the effects of genetic drift are more marked the smaller it is. Over time, as the population increases in size, the ongoing effects of genetic drift will tend to decline. However, by the time that occurs the population may have developed genetic characteristics quite distinct from the population from which it was originally drawn. These characteristics may even be so distinct as to justify this group being considered to be a separate species.

As noted above, it is what is happening at gene level that is seen as being of major importance. In particular, it is the characteristics of the gene pool that are important and how these might be changing over time. Theoretically, a gene pool is the complete set of different alleles possessed by a species as a whole. In practice, it may be understood as the set of different alleles available within a particular population. The larger the population, the more diverse that set of alleles is likely to be. It will provide greater genetic diversity and greater scope for novel combinations.

Even though the genes concerned are carried by individuals, little or no reference to those individuals tends to be made. To talk in population terms is something of an extension of the mathematical methods used to explore the ways in which gene frequencies change. It is possible to ignore the fact that the genes to be conveyed to the next generation do not exist except within the reproductive systems of individuals. Indeed, it is sometimes easy to overlook the fact that there are individuals at all and think of genes as discrete, even independent, objects. Indeed, each of the processes described above can be modelled mathematically in terms of genes alone. In such treatments, only the different gene frequencies within a population are considered. Here there are typically two underlying mathematical assumptions. Firstly, populations are theoretically infinitely large. Secondly, it is assumed that mating is completely random. Both are far from being the case in the lives of the individuals involved.

5. Randomness from Within

Random factors are often assumed to be of external origin. However, one important source of these effects comes, quite literally, from within: from the decisions made by the individuals concerned. This is particularly the case in higher animals. It is the individual that is very much implicated in genetic drift. It is the individual in possession of the genes that can be modelled mathematically that often chooses where to live and with whom to mate. For example, for a group to divide off from a parent population, as is the case in the founder effect, choice can play a role. This is especially the case in higher animals. This, then, has a direct bearing upon what happens eventually to the genes concerned. The effects of individual choice are often overlooked.

What description there is in current evolutionary biology of the way in which individual organisms live their lives tends to be somewhat 'averaged out'. For example, an organism's life is often seen in terms of life history events typical of all members of a species. In particular, these include consideration of the timing of key events relative to reproduction, such as the typical age when the first reproductive event occurs, the typical length of reproductive lifespan, the typical number of offspring. Indeed, the plan of a species' life history is seen as something that is itself open to natural selection. Typical behaviours such as mating patterns are those which receive particular attention. It is the adult phase that is of most interest since that is when reproduction takes place. However, while this life history approach has much to offer, life as 'lived-out' by each individual organism is something unique to that organism. Each organism is, after all, a discrete biological entity uniquely located in space and time. There is a unique set of influences brought to bear upon it; there is a unique set of choices it must and does make. These have direct effects on what it can contribute to the gene pool of the next generation. When it comes to understanding influences on the gene pool and how this may change and evolve, this should not be overlooked.

6. On The Question of Fitness-es

Fitness is a commonly used word in everyday language. Most often, it is used to refer to the physical quality of an individual; their ability to perform some usually physically active task. Frequently, the term is used in relation to an individual's athletic abilities. Fitness is also one of the central concepts of evolutionary biology but here it has more nuanced meanings. So much so that biologists are often at pains to make a clear distinction between the two.

In evolutionary biology, fitness represents an ability to survive and to reproduce. However, more often it tends to be thought of mainly in terms of reproductive success. Also, although it can be defined in relation to genotype or phenotype, it is more often genotype that is seen as the source of fitness i.e. of reproductive success. If an allele influences the ability to survive and/or reproduce, then its frequency will change over successive generations. An allele which increases its genetic contribution to the gene pool of the next generation will be considered fitter than one that does not. Thus, the notion of fitness is, in practice, a comparative one. Where numerical values are calculated, these are derived from ratios. Furthermore, there are different types of fitness which need to be differentiated.

The 'absolute fitness' of a genotype is defined as the ratio, in a given generation, of the number of individuals with a particular genotype after selection has taken place compared with the number there were before. Values greater than 1.0 indicate that that genotype is increasing in frequency; values less than 1.0 indicate that it is decreasing. 'Relative fitness' is the ratio of the average number of offspring, in a given generation, produced by a given genotype relative to the average number of offspring of another genotype. In practice, one genotype is typically used as a standard against which one or more comparisons with other genotypes are made. It was J.B.S. Haldane (1892-1964) – another of the key figures of the new evolutionary synthesis – who was the first to propose mathematical methods for quantifying fitness. Indeed, between 1924-1934, he published a series of ten academic papers under the general title 'A Mathematical Theory of Natural and Artificial Selection' in which he laid the numerical foundations for much of the new evolutionary synthesis.

A third form of fitness – 'inclusive fitness' – was developed much later. ‘Inclusive fitness’ was a concept introduced in 1964 by W.D. Hamilton (1936-2000) (Hamilton, 1964a, 1964b – although publication delays in fact led to the release of a description of inclusive fitness a year earlier (Hamilton, 1963)). Here, the genetic contribution made by an individual to the subsequent generation may not be as a direct result of reproduction but may come indirectly via a contribution to helping another to survive and reproduce. This finds particular expression in kin selection. Kin selection occurs when the actions of one individual leads to the survival and/or reproductive success of another individual with whom one is related (Maynard Smith, 1964). Where there is a kin relationship, there will be a genetic similarity between those related. The one providing the assistance will have genes in common with the one being assisted and so copies of one's own genes will also be being helped to survive in the process. Thus, altruistic acts which do not benefit the individual per se – and which may even be potentially hazardous to them – may be explained in terms of the benefit offered to shared genes. Even though there is a particular role played by individuals here, still the emphasis and ultimate explanation is given largely in genetic terms.

The notion of inclusive fitness further emphasises how the focus of evolutionary biology has come to be focussed at gene level. According to Maynard Smith (1989), '[f]itness is a property, not of an individual, but of a class of individuals'. By a 'class of individuals', he is referring here to a group of individuals each of whom have a given allele at a particular gene locus in common. That is, those who are homozygous for a particular allele at that locus. As before, the focus has come to be on genes in groups, not on the individuals in possession of those genes.

Not all individuals are equally successful when it comes to passing on copies of their genes. While some are abundant contributors to the next generation, some contribute much less. Some are even genetic dead-ends. Importantly, it does not necessarily follow that this is a reflection of the quality of the genetic endowment of the individual but may reflect other factors encountered during life. There is a need for more attention to be paid to what contributes to these factors. While no two organisms may encounter these factors in the same way and it is not possible to take all such factors into account, certain commonalities may be identified. From a plethora of stochastic factors, certain distinct characteristics may be identified.

7. Survival of the Fittest

Although fitness can be given a numerical value, it is usually better to think of it as a tendency or propensity. As a result of gene-centred thinking about evolution, that tendency or propensity has come to be a quality attributed to genes. However, that was not originally the case.

When, in his Principles of Biology (1864), Herbert Spencer (1820-1903) spoke of the 'survival of the fittest', he meant survival of those suited to their habitat or environmental conditions. He was not thinking of the survival of genes. Indeed, the concept of the gene had not yet been developed in its modern form. Neither was he thinking of reproductive success in the various guises presented above. Clearly, what Spencer had in mind was the survival of individual organisms. His was not the population-based or gene-based biology of the modern evolutionary synthesis. Furthermore, it was not a primarily reproduction-centred view either. It was a view which recognises the importance of the existence of the individual organism. This was essentially the view that Darwin held when proposing the idea of evolution by natural selection. Indeed, Darwin came to use the notion of 'the survival of the fitness' as equivalent to 'natural selection'. He came to include the phrase in the fifth and subsequent editions of 'On the Origin of Species'. Darwin and Spencer looked to the phenotype rather than the genotype. Thus, in addition to biological fitness as understood in modern terms, there is another form of fitness which may legitimately be referred to as 'Spencerian fitness' - after Herbert Spencer. This can even lay claim to being the original use of the notion. However, this type of fitness has been largely ignored and left under-developed. Here, fitness may be better understood primarily in relation to the phenotype of the individual. If one lacks fitness in this Spencerian sense of being suited to one's habitat, one's survival chances are likely to be impaired and, consequently, so too will one's reproductive chances. Here, the focus is on the individuals in whom the genes are located. It is, after all, via the individual as an organism that genes are transmitted from one generation to the next. Rather than thinking of a population of genes, one can think of a population of individuals showing different physical – that is, phenotypic – characteristics.

With too much emphasis on reproduction success, a subtle association between survival and reproduction is easily overlooked. Before one is able to reproduce one must first survive long enough to become sexually mature. Then, once sexually mature, the longer one survives and is sexually active, the more offspring one is likely to produce. This will mean a greater contribution to the gene pool of the next generation. Thus, an individual must not only have the ability to reproduce but also have as many opportunities as possible. In this, the life experiences of males and females in a given species will be different since each plays a different role in reproduction. These differences are impossible to take into consideration if thinking purely in terms of genes. The differences between males and females are missed.

8. The Phenotype

The phenotype is usually understood as an organism's observable characteristics or physical traits. This is not the same as simply its physical appearance – although this is certainly part of it. While the notion of the phenotype does encompass morphology at all physical levels – from macroscopic to microscopic – biochemical and physiological characteristics as well as developmental characteristics also form part of the phenotype. Furthermore, an organism's behaviour and the products of that behaviour may also be included. Indeed, the notion of the phenotype may be generalised to include all aspects of an organism other than its genotype.

Not all organisms with the same genotype are phenotypically identical. At best, they can only be said to be similar. Environmental effects on and during development mean that gene expression differs even between clones. In naturally occurring clones – such as monozygous multiple births (twins, triplets etc.) – the individuals, although similar, are never completely identical in any of their phenotypic characteristics. Indeed, it is now known that the fur patterns in experimentally cloned animals are not identical copies of the host animal (Shin et al., 2002).

The Danish botanist, Wilhelm Johannsen (1857-1927), was the first to make the distinction between genotype and phenotype – indeed it was he who coined the terms (Johannsen, 1911). Experimenting with the common bean (Phaseolus vulgaris), he found that in genetically identical plants, seeds were not physically identical. Instead, the phenotypic characteristics of seed size, he found to be normally distributed. While there was a cluster around an average value, there were also outliers. This range of variation he attributed to the position of the seed within the pod and the position of the pod on the plant. These different positions led to differences in the provision of resources to each seed during development which consequently affected their phenotype. Thus, the influence of the genotype alone was not responsible for the physical make-up of biological objects. External environmental factors were influential.

The distinction between genotype and phenotype echoes the distinction between germline and soma drawn by the German biologist, August Weismann (1834-1914). Weismann (1892) proposed that there was a distinction to be made between the sperm and ova – the germ cells – and the cells making up the rest of the body – the somatic cells. The germ cells held the heritable information whereas the somatic cells simply performed the tasks associated with keeping the organism alive. Furthermore, he proposed that there was a barrier between the two such that the somatic cells could not influence the germ cells. Nothing that happened to the somatic cells of an individual organism during its life could alter the information held by the germ cells. Variations that did occur in the heritable information – as is now known to occur via mutation – was confined to those cells alone.

However, while this so-called 'Weismann barrier' means that what happens to the body during its lifetime does not directly affect the germline, a more two-way interaction between genotype and environment is in play when it comes to the production of phenotypes. A phenotype is not merely the product of a set of instructions for manufacture contained within its genotype. A phenotype cannot be said to be a simple physical manifestation of a particular genotype. The organism that develops is the product of an interaction between the genes present in each cell and the environmental factors brought to bear locally on those cells as the organism develops. However, although a phenotype may be said to be the product of an interaction between genotype and environment, this is an over-simplification. The following simplistic expression in the form of an equation gives only an indication of how genotype and environment interact.

Genotype & Environment > Phenotype

Yet, this represents a common way of thinking about the production of phenotypes. While the range and nature of the interactions between genes and environment remain to be fully explored, one might do better by describing the phenotype as a constant interaction between genotype and environment.

Phenotype = [Genotype<>Environment]

Once the developmental phase has been negotiated and the adult stage is reached, that is not the end of the interactions between genes and environment. The genes in each cell are then involved in following a programme of continuing processes. These processes, depending upon what the environment provides for them, contribute to the survival of the organism as a whole, for good or ill. It is the environment which provides the substances which the body uses for energy, maintenance and repair. The phenotype – in the broad sense suggested above – can interact behaviourally with its surroundings and change its environment. Thus, the environmental effects on individual phenotypes can even be altered by the phenotypes themselves.

8.1 The Extended Phenotype

The notion of the extended phenotype was introduced by Richard Dawkins in the book of the same name (Dawkins, 1989). The notion of the phenotype need not be confined to just the individual organism but extended to include those alterations it makes to its surroundings in order to help ensure its survival. The notion recognises that animals in particular frequently alter their surroundings in order to enhance their survival chances. In this way, the phenotype and its survival are augmented in various ways. Examples of such extensions include the shelters and dwellings made by a variety of animals. Dawkins gives the particular example of the lodges and dams built by beavers which offer them protection from predators and provide them with a source of food – useful especially during the harsher times during the year. The species that can be said to have done most to extend its phenotype is humankind. Not only does it rely upon an extensive built environment within which to live, it also lives, for the most part, within different forms of clothing which allows it to exist in previously inaccessible parts of the world. However, Dawkins again takes a particularly gene-centred approach to the notion of the extended phenotype. The phenotype and its extensions he sees as primarily gene products directed at their own transmission from one generation to the next. Indeed, the book 'The Extended Phenotype' is sub-titled 'The Long Reach of the Gene'.

8.2 Phenotypic Plasticity and the Thrifty Phenotype

A significant characteristic of an individual's physical phenotype is its ability to change in response to environmental factors even during adult life. This is referred to as phenotypic plasticity. All organisms seem to have this capacity to some extent. It is usually considered more important for plants to show this capacity. They are, after all, immobile and so at the mercy of environmental change whereas animals, being more mobile, are more able to move or migrate or take other active steps to accommodate such changes, as appropriate.

The adult animal phenotype is open to numerous modifying influences. Significantly, environments are not constant. Seasonal variation is a characteristic of most parts of the world. This variation may range from minimal to substantial. Organisms need to be able to respond to the environment's lack of constancy. Some species do so behaviourally by migrating. Some become dormant for a season by hibernating (in winter) or aestivating (in summer). Those which remain active in the same habitat throughout the year may display physiological responses such as acclimatisation. Here, the individual, in effect, changes its phenotype temporarily. For example, the coats of some animals have different characteristic thicknesses and lengths at different times of the year in keeping with ambient temperatures. It pays for organisms not to be too phenotypically rigid in this respect but to be malleable even as adults. Were an organism not able to adjust, its chances of survival could be very much reduced.

The general notion of phenotypic plasticity has been extended in recent years to include the unborn. The thrifty phenotype hypothesis (or sometimes Barker's hypothesis, after its originator David Barker) suggests that during the prenatal period, foetal growth may be adjusted in keeping with the energy consumed by the mother. It is suggested that the mother physiologically modifies the development of the foetus. In particular, foetal growth may be sub-optimal when energy is limited. The foetus will be of reduced size compared with what it might otherwise have been had energy resources not been restricted. In effect, the foetus follows an alternative developmental trajectory; one that is more suited to the privations of the external environment which it will eventually encounter. By so doing, the mother produces offspring which are of a smaller body size with lower metabolic requirements. The mother, in effect, prepares her foetus for the world it is likely to face after birth (Bateson & Martin, 1999). As a result, after birth the neonate will not require more resources than are available in order to survive. Similarly, it will be on a developmental trajectory that will lead to an adult phenotype that does not require more resources than are available in order to survive. The mother is not, in any sense, doing this deliberately. Instead, there is an interaction of different systems within the mother which work to the ultimate advantage of the developing foetus after it is born. This interaction is itself a product of natural selection.

However, there is a potential disadvantage to this. The effect can be to make the foetus in question more susceptible to certain chronic conditions later in post-natal life should conditions change. Ailments including type 2 diabetes, coronary heart disease and hypertension are believed to result when, instead of encountering the privations for which the foetus was prepared, abundant resources are found instead (Barker, 1992).

Noticeably, in recent centuries and during the twentieth century in particular, the average height of males and females in different Western industrialised countries has increased (Komlos, 1998) – the effects of two world wars notwithstanding. A maximum height now appears to have been reached, the trend having levelled off somewhat. However, what this suggests is that until fairly recently, circumstances have not favoured the attainment of the full human height potential. The growth shown by individuals in the past has been sub-optimal.

It is possible to experimentally depress growth and the size that an animal can attain upon reaching adulthood. For example, animals raised in hypoxic environments (Hunter & Clegg, 1973a, 1973b) have been found to be smaller on average than their litter mates raised under standard control conditions.

8.3 Adult Phenotypes

The phenotype undergoes its greatest changes during the periods of foetal and post-natal development prior to reaching sexual maturity. During the reproductively active adult period, the phenotype does not undergo major structural change or reorganisation. In the study of anatomy and physiology, it has been the adult phase that has been considered the typical phase for study. This, it may be argued, is a form of 'adultism' – a focus on the adult period at the neglect of other periods. As noted above, once the developmental stage is complete and adulthood is reached, the phenotype is not static. What has been put into place must be maintained. Also, the phenotype is able to undergo changes in response to energy availability. In times of excess, more may be consumed and what is not used stored within the body, typically as fat. In times of want, what has been stored previously is released to provide usable energy. Thus, the individual is able to put on and lose weight accordingly. This often has the effect of changing the individual's outward appearance and sometimes physical agility.

The body also has processes which act to restore the physical integrity of parts when they are injured. Wounds and minor injuries are healed. However, permanent alterations may result depending upon the nature of the injury incurred and the extent and success of healing. Extensive scarring and misaligned healed broken bones can lead to a limitation in the range of movement available. The use of certain parts of the body may be permanently altered or even lost. In such instances, it is possible for compensatory changes to result. Some parts may hypertrophy as they come to be used to compensate for the loss of use elsewhere. At the same time, damaged parts no longer used as before may atrophy.

The most marked change in adult phenotype occurs in relation to the pregnant female body. The pregnant phenotype is, for the individual concerned, a temporarily new phenotype. In this instance, it is not merely the product of a gene-environment interaction but the product of two gene-environment interactions: that of the mother and that of the foetus. The range of activities that the pregnant female is able to perform gradually changes during the pregnancy. Pregnancy is a hazardous time for all such animals, even for those humans who have the benefit of clinical assistance. It is particularly hazardous for those humans and animals that live in more natural settings. The ability to survive pregnancy appears to be a combination of a number of factors. Among these, genetic factors such as the immunological compatibility of mother and foetus, the quality of the mother's pre-existing phenotype and her ability to support a growing foetus and her continued ability to negotiate the dangers of the environment are each important.

It is not unreasonable to suggest that there are three phases to human life. These may be described as pre-adult, adult and post-adult. The adult phase is that associated with sexual maturity and reproduction. The pre-adult and post-adult phases are both non-reproductive phases. The adult phase is the phase to which evolutionary biology tends to give the most attention. This is perhaps understandable. It is, after all, the only phase during which genes can be transferred. However, the pre-adult phase is, in many respects, a phase in preparation for reproduction. What happens to the individual during that phase may have a bearing on its ensuing reproductive history. While in some animals, the post-adult phase is that phase when reproduction and the activities associated with it have ceased, there may still be a role to be played by these individuals. For example, in humans, the care and nurturing of infants may be switched from one's own children to that of one's children's children. This may be seen as another example of inclusive fitness.

The adult period is not a perfect plateau during which the organism is in the prime of life. Arguably, this is a period of often imperceptibly slow decline. Either way, it is a period of time during which there is a concerted resistance, by the organism as a system, to the inevitable decline into entropic decay. Ultimately, no organism is immortal. The post-adult phase is characterised by a steeper decline and decay with regard to systemic integrity than was previously the case.

9. Sexual selection

The idea of sexual selection was introduced by Charles Darwin in 'On the Origin of Species' as an aspect of natural selection. However, it was only given a treatment of a few pages. Darwin later extended these ideas, as well as applying them to humans, in his 'The Descent of Man and Selection in Relation to Sex' (Darwin, 1871). Although initially linked, natural selection and sexual selection are nowadays often treated quite separately.

The subtitle of 'On the Origin of Species' was 'the Preservation of Favoured Races in the Struggle for Life'. In the 'Descent of Man' the idea of that struggle was extended. Natural selection involves a struggle to survive. Sexual selection involves a struggle to reproduce – what Darwin called the 'sexual struggle'. This 'sexual struggle', he noted, was of two kinds. In one kind, the struggle was between individuals of the same sex. This was generally between males who sought to drive away or kill rivals in a competition for access to females with whom they wished to mate. Here, while the males competed, the females remained largely passive. In the other kind, the struggle was, in effect, between the sexes. Members of one sex would seek to 'excite or charm' (Darwin, 1871) those of the other sex. Those affected in this way were generally females. This time, they were not passive but involved in making a choice as to which male with whom to mate. What competition there was between males was not a matter of direct aggression but of demonstrating individual prowess.

The concept of sexual selection sprang from the recognition that many animals develop phenotypic characteristics which do not aid survival directly but may even become so exaggerated as to potentially hinder survival. These features clearly served some other role. As noted earlier, mating does not occur at random. It transpires that the role played by these exaggerated features is one of ensuring the best possible mating chances in different ways.

Where males compete with each other, this is sometimes described as 'intra-sexual selection'. The 'selection' of a successful mating partner for a largely passive female is effected by one sex only: the males. Thus, this is sometimes also called 'male-male competition' selection. Some phenotypes, such are the Irish elk's huge antlers (Gould, 1974; Moen et al., 1999), serve to beat rivals for access to females by intimidation, deterrence or defeat in contest.

Where females choose the male with whom to mate, this is sometimes described as 'inter-sexual selection'. This is also known as 'mate choice' or 'female choice' selection. Here, the choice is based upon an assessment made by the female of some quality or ability displayed by the suitor. Birds, for example, may display plumage with vivid colours or produce elaborate songs. Others may perform some form of dance to attract a mate or they may build a nest which the mate finds to its liking as somewhere in which it can raise a brood of chicks. Famously, the peacock has an extremely elaborate tail (or train) which he uses to attract a mate. It appears that the physical qualities of a peacock that can produce an elaborate and symmetrical tail with a fine array of feathers gets a more favourable response from a peahen than does a peacock without such a train. The peahen is geared to respond to signals which indicate that the peacock is of better physical quality and it is assumed, by proxy, better genetic quality (Petrie, 1994).

Taking a gene-centred approach, both forms of sexual selection can be understood in similar ways. It may be argued that genes that make good quality individuals able to succeed in combat or be attractive enough to lure a mate are also genes that can make offspring of a similarly good quality. Suitors made by and in possession of such genes are those that will succeed in both intra- and inter-sexual selection. To show that they are made by such genes and, therefore, have them available to pass on to offspring they might sire, certain phenotypic characteristics are expressed. In both cases, it is the quality of the phenotype that really matters.

9.1 Individual Quality

Both intra- and inter-sexual selection are processes that are fundamentally about the phenotypic quality of the individuals concerned. This, in turn, is understood to represent a measure of the genetic quality of the individual concerned. However, this tends to overlook the fact that an individual's phenotype is not static during adult life - the period when reproduction takes place. Adult life may be characterised by a period when the animal's physical state is relatively stable but this does not last indefinitely. Males that have previously been successful in combat against many potential usurpers and those whose elaborate plumage has previously attracted many females both get to a point in their lives when they are no longer as successful as before even though they may be able to continue to reproduce. Phenotypically, they are no longer the fine physical specimens they once were. The ability to win in combat or to maintain one's plumage declines with age. Indeed, the ability to win in combat may decline due in part to the injuries sustained in having won earlier contests. Genetically, however, such individuals are the same as ever they were. This is one of the lessons to be learnt from Weismann. Although the phenotype declines, the genotype does not. The vehicle that is made by genes is no longer maintained by them. The body ages and decays while the genes do not.

9.2 Reproductive Acts

Sexual selection, as described above, is only part of the struggle to reproduce. More accurately, it is about gaining the opportunity to mate; to perform reproductive acts of some kind. Performing a reproductive act is not the same as reproduction per se. By a 'reproductive act', one is referring to acts which an individual must perform prior to the conception of offspring. Only human beings seem to be aware that copulation can result in pregnancy and childbirth. Only they appear to know that certain acts may result in the reproduction of their kind. In most other animals, the innate desire is not to reproduce as such but rather to perform 'reproductive acts', to engage in copulation and associated activities. What results from this is a quite separate matter. The animal may be quite unaware that there is any association between the birth of offspring and an act performed at some time in the recent past. 'Reproductive acts' should, perhaps, be considered separately from the rest of reproduction. It is by no means certain that such acts will be successful in bringing about conception or in producing live or viable offspring. Individuals may even be sterile and their unions with others, therefore, infertile. Yet, there may be no outward phenotypic indication that this is the case.

10. The 'Struggle for Life'

Darwin (1859) spoke of two struggles: the struggle to survive and the struggle to reproduce. In order to hope to be successful in the latter, one must first be successful in the former. Those unsuccessful in the former are often assumed to have been unsuccessful because of their poor genetic quality. That being the case, they are the victims of natural selection. They are weeded out of the gene pool, their poor quality genes with them, thereby reducing the frequency of those genes. This is, indeed, often the case. However, sometimes a lack of success in survival is a matter of accident or bad luck, the result of being in the wrong place at the wrong time when, for example, a predator strikes.

The two struggles of which Darwin spoke may legitimately be referred to as the two 'Darwinian imperatives'. It is imperative that individual survival and the performance of reproductive acts are both accomplished successfully for the reproduction central to evolution to ensue. Without reproduction and the concomitant gene transfer, no evolution within a species is possible. Offspring are the ultimate end product of a series of events. Importantly, they result from two individuals having survived long enough to reach sexual maturity and being able to perform reproductive acts. Both survival and performing reproductive acts are important in their respect ways. Failure in either can lead to an individual failing to contribute genes to the next generation. Understanding factors which influence the relative success of accomplishing the 'Darwinian imperatives' is clearly important. Many of these factors are associated with the life of the individual as it is lived out. The precise details of these will differ depending on the species and the circumstances of the individuals concerned. However, what is clear is that looking at the gene or population level loses sight of this.

10.1 An Inner Struggle

Not all phenotypic characteristics pertinent to survival have received attention. While physical and behavioural characteristics have received attention, less tangible phenomena have not. For higher animals, an important aspect to the struggles in which it must engage is how the animal feels within itself, that is, the state of its sense of self-awareness. These feelings impact both positively and negatively on how the individual goes about its daily living and how it ensures its survival. Going about the performance of reproductive acts and how successful these turn out to be are also likely to be affected.

The internal experience of non-human animals is not open to human scrutiny. Indeed, neither is that of other humans. One's inner experience is known only by oneself. However, one can infer the presence of an interior world from the behaviour and demeanour of a range of animals. While some may even try to enter that world via an act of the imagination, that is not what is advocated here. Such subjectivity is not typical of the modern scientific approach and may even be frowned upon. However, that is no reason for not trying to look into the role that self-awareness plays in the lives of others – human or non-human. One is aware from personal experience that one's ability to go about daily life can be greatly affected by a number of different factors which impinge upon inner experience. For humans, many of these relate to emotional states which one cannot be sure are possessed even by the higher primates. However, there are experiences which one can reasonably suggest are experienced by a range of non-human animals. For example, it is reasonable to suggest that animals experience hunger and thirst, feelings of being too hot or too cold and that they are also able to experience pain and discomfort. As such, it might be argued that inner experience – one's sense of self-awareness – is an aspect of the phenotype too and applies to both human and non-human animals.

Unsurprisingly, this has not featured significantly in evolutionary biology for the reasons already noted. However, they do have perhaps a tacit presence. It is the experience of hunger or thirst which leads an animal to eat or drink. The feelings of hunger and thirst are essential for survival. Without them, no higher terrestrial animal would know when to take in the substances necessary for life. Similarly, responses to feelings of being too hot or too cold are essential. All organisms must remain within a certain temperature range in order to survive. This range is a product of an animal’s physiology. From human studies, it is evident that feelings of being too hot or too cold coincide with deviations outside optimal physiological temperature ranges (Case & Waterhouse, 1994). Thus, these feelings ensure that the appropriate physiological temperatures are maintained. These inner experiences are not constant. They vary with the physiological state of the individual concerned. Feelings of hunger and thirst last until, having eaten or drunk, one is satiated. Feelings of being too hot or too cold, last until one returns to a state within the optimal physiological temperature range.

As already noted, behaviours may be thought of as aspects of the phenotype. That being the case, behaviours such as eating and drinking are also phenotypic expressions. One can also infer some inner experience akin to the human experience of hunger or thirst to be evident in non-human animals which brings about this behaviour. Similarly, self-awareness and the specific experiences which lead to the expression of these behaviours may also be considered to be phenotypic.

In relation to reproduction, what triggers the desire to mate is a complex matter. A whole variety of factors not necessarily obvious to the observer or the participant are involved. In some species, this seems to be linked to the time of year with external environmental factors seemingly involved. Here the season of birth coincides with those times of the year which are less hazardous for the survival of the newborn. That being the case, the time of mating has become linked to a time of year appropriately in advance of the season of birth. Chemical signals via pheromones, for example, also appear to trigger the desire to mate. Whatever is the case for non-human animals, in humans, it is clear that libido is not constant, either throughout life or over shorter time periods. Libido is higher in the years after sexual maturity is first reached than it is during childhood or later life. There also appear to be times of the day when reproductive acts are more commonly performed than at others. While there may be, in humans, social factors involved, there is also the suggestion that there may be a circadian element (Refinetti, 2005). As well as not being constant for a given individual, different individuals also seem to have different inherent levels of libido. In some, it may be quite high; in others, it may be quite low.

11. Evolutionary Landscapes

The new evolutionary synthesis led to a new way of approaching evolution. The former focus on the physical nature of organisms typical of the Victorian naturalist gave way to a focus on the transmission of genes – the particles of inheritance. Organisms took on a somewhat secondary importance. They were merely the products and purveyors of genes. What evolved was not the organism but the gene pools which gave rise to those organisms. In particular, it was gene frequencies within a gene pool that changed – evolved – over time. Focusing on the gene frequencies within the gene pool, numerical and other models of genetic change became possible.

In the early 1930s, Sewall Wright proposed the notion of the adaptive landscape (Wright, 1932, 1980, 1988). This was primarily a theoretical tool – a heuristic for evolutionary biology – aimed at describing how different alleles can become more or less frequent within a population (Pigliucci, 2008; Provine, 1986). As such, it was also a way of illustrating natural selection in action. Wright's adaptive landscape consisted of a contoured surface – rather like a relief map – demonstrating how different gene combinations could be more or less beneficial than others.

With two axes representing two different genotypes or alleles (Figure 1), different interactions would lead, Wright suggested, to more or less (in his words) 'harmonious' combinations under certain circumstances. Thus, the map represents areas (or peaks) of adaptation (denoted by a '+' sign) and other areas (troughs and valleys) of poor or non-adaptation (denoted by a '-' sign). The higher up on one of these landscapes the better. Being higher up, an allele combination was considered as being genetically better adapted than one represented lower down. Wright's original formulation saw specific allele combinations as being represented by single points plotted on the landscape while populations were represented as clouds of points.

Figure 1. An adaptive landscape (Redrawn after Wright, 1932).

As Wright recognised, this model was a considerable simplification. There were in reality myriads of different allele combinations that could arise. However, using just two, Wright was, nevertheless, able to make an interesting case. Indeed, the notion of the adaptive landscape has been described as probably the most influential heuristic in evolutionary biology (Slipper, 2004). Part of its appeal lies, perhaps, in it being a visual metaphor rather than a series of mathematical formulae. It certainly has an abstract or conceptual appeal as a pictorial way of representing something otherwise highly complex. Furthermore, it continues to attract attention in a quest for development and improvement (Calcott, 2008).

11.1 Which Landscape?

Although the term ‘adaptive landscape’ is commonly used, so too is the term ‘fitness landscape’. The concepts of ‘adaptation’ and ‘fitness’ are often used synonymously and interchangeably. However, although this does not tend to be problematic as such, it may be useful to draw a distinction between ‘adaptation’ and ‘fitness’.

When a species is said to be 'adapted', it is to a particular set of environmental conditions. Since selective pressures brought to bear on the phenotype by that environment have the ultimate effect of changing the gene frequencies within the population, the adaptation is seen as primarily at the level of the gene. This view is not entirely wrong. Certainly, the overall architecture of an organism and key aspects of its physiology which dictate the type of environment within which it can survive is a product of its genotype. However, in terms of the different types of 'fitness' described earlier, perhaps that most suited to a representation on a fitness landscape is 'Spencerian fitness'. Here it is the level of the phenotype that matters: the characteristics that are being displayed by the individual organism as it interacts directly with the environment.

In addition to the use of landscapes to depict allele combinations, the same approach has been adopted to represent phenotypes. In 1944, the American palaeontologist George Gaylord Simpson (1902-1984) proposed a notional landscape based upon phenotypic characteristics (Simpson, 1944, 1953). Graphically, phenotypic landscapes have much the same appearance as adaptive landscapes. The difference comes in that the determinants of the contours are quite different. Instead of genotypic features, it is a range of phenotypic characteristics that gives the terrain its contours. It is an individual's particular phenotype which determines its position on that terrain. The extent of its phenotypic adaptation to the environment in question determines whether it is higher or lower on the landscape. Although Simpson did not use the term, these phenotypic qualities may be thought of in terms of the 'Spencerian fitness' described above.

While Wright's adaptive landscape, based upon genotypic combinations, was theoretically acceptable, Simpson's use of phenotypic traits is perhaps conceptually more satisfying. Physically discernable characteristics relating to the quality of the individual, not least in relation to a given environmental context, can be more easily discernible, thereby making this approach intuitively more satisfying. Unfortunately, this aspect of Simpson's work has been overlooked somewhat. It is worth remembering here the modern definition of a phenotype as being any observable characteristic or trait of an organism. Thus, this landscape includes anatomical, physiological behavioural and, as suggested above, the inner experiential properties of the individual. What these phenotypic characteristics have in common is their joint contribution to the individual's overall survival chances. Here, multiple factors are expressed in a single qualitative notion.

12. Evolutionary Medicine

Evolutionary medicine (originally Darwinian medicine) is the relatively new science of applying evolutionary ideas to medical problems. Originating in the early 1990s (Williams & Nesse, 1991; Nesse & Williams, 1994, 1995), it has advocated explaining medical problems in 'ultimate' as well as 'proximate' terms. That is, a medical condition should be understood not only in terms of causes-and-effects but more deeply. It should be understood in terms of why one is susceptible to a given condition in the first place. Thus, evolutionary medicine has been defined as 'the enterprise of trying to find evolutionary explanations for vulnerabilities to disease' (Nesse, 2011).

The Ukrainian-born evolutionary biologist, Theodosius Dobzhansky (1900-1975) famously proposed that 'nothing in biology makes sense except in the light of evolution' (Dobzhansky, 1973). Nesse and Williams (1994, 1995) adopted and adapted this, suggesting that 'nothing in medicine makes sense except in the light of evolution'. For a number of years, the proponents of evolutionary medicine have advocated the teaching of evolutionary biology to medical students (Nesse, 2001a, 2001b; Nesse et al., 2006, Nesse & Williams, 1997). This has met with limited success. Instead, anthropologists have tended to be more enthusiastic adopters of the tenets of evolutionary biology than clinicians (Lewis, 2008). As currently construed, evolutionary medicine looks less to the needs and problems of the individual and more to population-based explanations of the vulnerabilities to disease. It has, so far, had relatively little to offer the individual patient in a clinical setting other than a way of explaining why they or a member of their family is suffering in some way. While this may help put matters into a historical perspective, it does not necessarily help solve the patient's immediate problems.

It is at the level of the phenotype that the question of the place of evolutionary biology in the understanding of the concepts of illness, disease and health arises. It is the phenotype that shows the physical signs of a medical condition and where the symptoms are experienced. Indeed, feeling ill or unwell and experiences of pain and discomfort may also be considered as part of the phenotype as suggested above. Furthermore, these experiences may have survival advantage in that they elicit responses that counter what may be detrimental to the well-being and even the survival of the individual.

As yet, there is no notion of the individual in evolutionary medicine even though that is what clinical medicine is primarily concerned with. This is perhaps also a product of the fact that there is no theory of the organism as an individual entity in evolutionary biology. It is only via a clinical concern for the individual that public health and epidemiology have any significance. As already noted, since Darwin's time, attention has shifted from organisms to genes and populations. It may well be to the benefit and advancement of evolutionary medicine that an individualised approach be developed.

One way in which this might be achieved is via a consideration of the phenotypic quality of the individual in terms of their survival chances. A healthy individual is likely to be one that has a good chance of continuing to survival – changes in the environment notwithstanding. An unhealthy individual is one whose survival chances are not so good. If the overall phenotypic quality of an individual can be represented meaningfully, then this may bridge the gap between clinical medicine and evolutionary medicine.

12.1 Less Than Fit

Currently, in evolutionary biology – and indeed biology in general – there is no theory of the organism as an individual entity. Instead, when organisms are described, it is in what might be described as canonical terms (Smith & Kumar, 2005). That is, the typical anatomical and physiological features and characteristics are presented. This means that anatomical anomalies and variants and physiological responses to unusual and extreme conditions are largely missing, left instead for separate consideration. For evolutionary biology, this may be a potentially significant omission. It is via the pressures brought to bear on phenotypically different individuals that natural selection operates. In that way, some leave more offspring on average, some leave fewer. However, it is one thing to recognise differential reproductive success and quite another to understand what this means in terms of the life of the individuals as lived on a day-to-day basis.

All organisms must contend with illness, disease and injury. These are characteristic features of life. The longer one lives, the more one is likely to encounter them. That any animal has ever lived a fully healthy life from beginning to end is perhaps inconceivable. Yet, despite this, these features do not figure highly in general or evolutionary biology. Instead, they tend to be treated separately as the preserve of the medical and veterinary professions.

In relation to evolutionary biology, illness, disease and injury can even have an effect not unlike genetic drift. Depending upon the size of the population concerned, losing members to an infectious disease may produce a genetic bottleneck. This will then have a bearing on the gene frequencies that can be demonstrated by ensuing generations. Not all individuals within a species are equally susceptible or prone to the same illnesses or diseases. Neither are they equally prone to injury. While differences in each individual's immune system can explain the former, the latter can be explained in terms of age- and sex-related behavioural patterns. Younger animals tend to be more active and adventurous than older animals. Furthermore, males tend to be generally more adventurous than females. Human males, for example, tend to experience more accidents as a result of playing sports, fighting and driving. This is also manifested in age- and sex-related death rate statistics. While the selective pressures exerted by a given environment may be said to include infectious agents and their ability to withstand their effects may be seen as part of being genetically adapted, the desire to engage in behaviours that cause death and injury by accident comes from within the individual. Many young individuals that are otherwise well suited to their environment perish as a result of such desires and not as a result of being otherwise maladapted.

For humans, the number of medical and related problems which can hinder individual survival and/or the ability to reproduce is large. The number of conditions listed by different classification systems (e.g. The International Statistical Classification of Diseases and Related Health Problems or The Systematized Nomenclature of Medicine) runs into many thousands. Each individual clinical condition cannot be taken into account separately. However, as noted above, it is possible to make certain generalisations which allow the individual to be given greater attention as a biological entity within an evolutionary context.

13. The Concomitants of Survival – A 'Survival Triad'

For purposes of understanding the individual organism more fully in terms of evolutionary biology, a more fully developed theory of the individual organism is necessary. Central to this is an exploration of the first of the two Darwinian imperatives described above: the struggle for life – survival. Being able to survive – succeeding in the struggle for life – is a product of a variety of factors. This includes how well one is adapted to one's environment but it also includes how well one is able to contend with illness, disease and injury as part of that environment. It is not necessary to account for each separate factor that influences survival. Instead, these factors may be distilled into three distinct sets. These represent three fundamental and concurrent aspects of organismal life (Lewis, 2011).

These are:

· The individual's physical state – how well it is operating as an organic system.

· The individual's 'experiential' state – how it is known or represented to itself.

· The individual's 'behavioural' state – how well it is able to interact with the environment in which it finds itself.

These three concurrent features are essential for individual survival. Firstly, organisms must have an orderly physical, that is, an orderly anatomical and physiological organisation. Too often, organisms are thought of as merely physical objects – albeit of a special kind. Instead, they should be thought of as systems consisting of physiological processes which give rise to orderly physical forms – not as physical objects within which there happen to be physiological processes occurring. However, to be a living organism, anatomical and physiological organisation is not enough. Numerous interlinked internal physiological processes must be maintained. The organism must be operating as an integrated system. This requires a form of self-referential communication or internal information flow to occur. In this way, the integrity of the whole organism is maintained as an active system. In sentient beings, such as the higher animals, some of this information flow reaches the level of consciousness; there is a degree of conscious self-awareness which is used to survival effect. For example, as noted above, responses to feelings of hunger and thirst, of being too hot or too cold, of pain and of being ill, have survival benefit. These are, in effect, important forms of information about physical state requiring different responses in order to ensure continued survival. Furthermore, the organism is not a closed system; matter and energy flow through it. Things like food and drink are essential for survival and must be obtained externally as these are the sources of that matter and energy. Thus, an organism must be able to interact with its surroundings physically in order to ensure that its needs are obtained.

These three features – which may be characterised as physical, experiential (or informational) and behavioural (or interactional) states of the individual – operate concurrently. They constitute what might be described as a Survival Triad (Lewis, 2011). Failure in any one or more of these aspects will compromise the organism's ability to survive.

Of these three sets of factors affecting survival, inner experience – one's awareness of oneself – has, as noted above, not figured at all highly in evolutionary biology. It is impossible to study that to which one has no access: the interior world of the individual animal (human and non-human). However, some clues may be obtained from looking at the behaviour and demeanour of others and from relating this to what is known from shared human experience. Within limits, this may also be considered to be shared animal experience. Therefore, it is worth considering this further.

One's experience of oneself – one's sense of self-awareness – may, it was suggested, be viewed as a phenotypic characteristic. Consciousness is usually considered to be an emergent property. However, for it to have established itself as an organismal property, it is reasonable to expect that this phenomenon has a survival benefit. This benefit is likely to be in relation to what it tells the organism about itself and the behaviours it elicits to ensure survival. It is important that the physical state of the body is maintained within certain limits. Responding to self-experience ensures this. The experience that humans call thirst is a way of the body's physical state of hydration making itself known to itself and bringing about drinking. Hunger is similar, although with not quite the immediacy that thirst requires. It is necessary to ensure an input of energy and the physical components necessary for bodily maintenance and repair. Not getting too hot or too cold ensures that the temperature range within which the body's physiological processes are performed is maintained near the optimum. The experience called illness is similar. It too elicits responses which can be understood as directed at ensuring individual survival. Illness behaviour (McHugh & Vallis, 1986) is a product of the interior world of the individual. These behaviours include becoming less active, sleeping, finding a way of keeping warm, preferring certain foods and avoiding others – or avoiding food altogether. These are illness behaviours that can be observed in animals (Engel, 2003). In humans, this is something with which all can identify from one's own experience.

Self-awareness offers the physical body many survival advantages. This quality of the organism has become particularly elaborate in human beings. Whether there has been some runaway effect here producing a form of self-awareness or consciousness that exceeds what is necessary for basic survival is a moot point. For example, reading these words is unlikely to have a direct effect on ensuring one's survival. Writing them certainly did not. Human consciousness now offers much more than that which is strictly necessary for survival. However, there should, perhaps, be greater prominence given to the importance of self-awareness or consciousness for survival.

13.1 Describing the State of the Individual Organism

As with other notions in evolutionary biology, discussed above, the survival triad representing the three concomitants of survival can be described graphically. Here three orthogonal axes may be used. Each represents one of the three aspects of the triad (Figure 2).

Figure 2. A Survival Triad.

The horizontal axis represents the physical state of the individual organism, the vertical axis its experiential state and the third (z) axis its behavioural state: its ability to interact with its environment. However, the notional scale used for each axis is not as typically laid out. The horizontal axis represents the level of disorder in the body as a physical system. The vertical axis represents the level of disturbance there is in the internal informational and experiential state of the individual organism. The z-axis represents the level of behavioural constraint there is upon the individual in terms of how it is able to interact with its environment and how well it can go about the activities essential for survival. Importantly, the axes are set out to represent increases in that which is detrimental to individual survival – not what is of benefit to it. Increases along the horizontal and vertical axes are increases in the physical and information entropy within the organism as a system. Increases along the z-axis, are, in effect, decreases in the ability to perform tasks aimed at staying alive. This may be due either to a feature of the individual in question or due to something about the environment. For example, an individual may not be able to obtain water because of an inability to walk to a source of water or, being able to walk, finding that the source has dried up. In both cases, the individual will be unable to drink. This, in turn, will have an adverse effect on the body as a system as it will increase physical disorder. As these physical processes are increasingly affected, the experience of thirst will become increasingly more distressing.

The further one moves along each axis (in the direction of the arrows), the greater the risk to individual survival. By notionally plotting a measure of the physical, experiential and behavioural state of an individual, some idea of the overall state of that individual can be depicted in the phase space within the limits of the axes. The closer one is to the origin, the better.

Just as the idea of the adaptive landscape was not a strictly numerical notion, so too, this model of the organism is not meant to attract specific numerical values. It is meant as a way of envisaging the individual organism via a mental image or heuristic. By so doing, it represents the organism more fully; it draws attention to the fact that there are three sets of factors acting concurrently on the organism and, at the same time, manages to unify these into a single point representing the individual's survival chances – unforeseen eventualities notwithstanding.

13.2 The Organism 'in Isolation'

Taking just part of the survival triad, the system state of the organism 'in isolation' may be represented. The organism is, in effect, a self-referential, self-organising material system maintaining itself in the face of its inevitable entropic demise. It does this by interacting with its environment. However, this latter capacity is typically omitted from textbooks of anatomy and physiology. Therefore, assuming, as these textbooks do, that this interaction (in terms of the z-axis (Figure 1)) is not restricted, the organism may be represented separately – 'in isolation' – by using just the horizontal and vertical axes. Laying these axes flat, for convenience, it is possible to present a 'survivability surface' representing the ability of the organism to continue to survive – ceteris paribus (Figure 3). As before, the closer one is to the origin, the better. That is where states most conducive to survival are situated. Taking these two axes in isolation provides an alternative, more integrated way of thinking about the organism. (For the development of a full theory of the organism as an individual entity, the factors relating to all three axes must be considered.)

Figure 3. A Survivability Surface.

Based upon the x (Physical Disorder) and y (Experiential Disturbance) axes of Figure 2.

14. Combining Different Models

A notional evaluation of each of the three concomitants of survival can be used to plot a representation of the overall state of the individual in three dimensions (Figure 4). This is a representation of the survival chances of the individual. This triad, therefore, offers a notional representation of the Spencerian fitness of the individual as an entity. It is a largely phenotypic evaluation of that individual. That being the case, the triad also represents something that can be translated onto a phenotypic landscape. If the individual can be represented close to the origin of the triad diagram, then that individual will also be close to their respective peak on the phenotypic landscape. The further they are from the origin, the further they will be from such a peak.

Figure 4. A notional representation of the overall state of an individual in terms of their degree of

physical disorder (x), experiential disturbance (y) and behavioural constraint (z).

There is, however, a tacit feature of these landscapes that must first be addressed. What both the adaptive and phenotypic landscapes represent is depicted in somewhat static terms. The organisms represented are unchanging. This is not a representation of real-life. An old, sick or dying individual, using Wright's original version of the adaptive landscape, can be represented, genetically, at an adaptive peak. However, while, in evolutionary terms, one can see Wright's point – that the individual's genotype is well adapted to a given environment – at the same time, that individual, in strictly phenotypic terms, cannot be deemed to be at any sort of peak or optimal state. Indeed, it is in a sub-optimal state that all organisms actually live out their entire existence. A gene-based adaptive landscape is perhaps misleading in this respect. One based on phenotype is more realistic. Such a landscape can also be used to include changes that occur during life. One must be able to include the scenario where an individual may be genetically adapted to a given environment but still fail to be completely suited to it as a result of phenotypic changes due to age, pathology, injury or some other mishap. The phenotypic quality of the individuals that make up a population is perhaps more significant than is usually realised. As the foregoing discussion has highlighted, an individual's phenotype is not a simple product of its genotype alone. Neither is it a single fixed thing, even during an apparently stable phase of its life. These types of change have not, so far, been built into notions of an evolutionary landscape. However, the phenotypic landscape is able to accommodate this.

Organisms do not possess a single unchanging Spencerian fitness and are not, therefore, represented by fixed points on a fitness landscape but by moveable ones. Just as their state changes during life, so too will their position within the triad diagram (Figure 4) and on a phenotypic landscape. To be completely accurate, a phenotypic landscape should include all the phenotypic states possible for a given individual. That individual will exist at different points on the landscape at different times. Each point represents the fitness or survival chances associated with a particular phenotype. Later in life, the individual will descend into one or other trough or valley on the landscape as their phenotypic state becomes increasingly less viable. It is these real-life states that the model of the triad seeks to describe.

15. Agent-based Evolutionary Models

The original mathematical models of the new evolutionary synthesis, as developed by Haldane and others, understandably used the mathematics and calculating methods of their time. One should not fall into the trap of assuming that these methods give a complete and perfect description of evolutionary processes. These methods were only tools with which to explore the process of evolution. Since they were developed, there have been developments in numerical techniques, not least in computer-based modelling, which offer new options for evolutionary biology.

Indeed, computer science has not been slow to use the concept of evolution for its own purposes. One of the central features adopted is that of iteration. This is the act of repeating a process or mathematical manipulation over a number of cycles. Sometimes this is allowed to continue until a certain desired end-point is reached. Alternatively, the process of iteration may be left to run indefinitely in order to observe what emerges over different periods of time. Evolutionary biology is a fundamentally iterative process. Each generation is, in effect, a new iteration.

In this respect, evolutionary biology should be able to borrow ideas and techniques from computer science. In particular, techniques using 'autonomous interacting agents' have been developed that may be of particular use in the study of evolutionary processes. Here, discrete entities – or agents – exist within a mathematical framework. These agents are able to behave independently in accordance with some predefined rules in a quasi-intelligent way. Having been given a set of starting conditions, the agents are then allowed to interact with each other. Thus, instead of using mathematical methods which assume population size to be infinitely large and mating to be completely random and which lose sight of the individuals within populations as a result, it is now possible to set up populations made from individual agents which, in effect, live out individual lives. Given different starting conditions and rules of behaviour and left to evolve by themselves, one then waits to see what emerges.

One of the features of agent-based computing models is that interacting agents can be of different kinds or qualities. By using an agent-based approach, different features and qualities of the individuals, such as their phenotypic qualities, can be introduced. Distinctions between male and female and between adults and non-adults can be introduced as can a host of other factors. In short, instead of just using methods which average out and lose the distinction between individuals, techniques are becoming available which can accommodate and build upon such differences. Populations of interacting individual agents can be modelled over any number of generations.

That being the case, in future it should also be possible to model evolution while taking into account each of the factors described by the 'survival triad'. This was ostensibly a representation of the individual organism in terms of the three key aspects of organismal survival. Individual agents can be programmed to vary in each of these aspects and, as a result, their overall state.

16. Conclusion

Given the time in which it was written, one of the hallmarks of Darwin's 'On the Origin of Species' was its emphasis upon what is now known as the phenotype. Upon the quality of an individual's phenotype rested its ability to succeed in the struggle for life; to be able to continue to survival and to be able to go about performing reproductive acts. This focus on the phenotype was further emphasised when Spencer spoke of differential survival favouring those best suited to their respective environments. Nineteenth century emphasis seems to have quickly receded from view with the emergence of the new evolutionary synthesis in the first half of the twentieth century. Accordingly, a gene-centred view of evolution grew up that has come to take precedence over any focus on the phenotype. Furthermore, that gene-centred view has had the effect of putting particular emphasis on reproduction since that is the means whereby genes are transferred between generations.

Individual phenotypes are not, however, the simple products of genes – external factors also influence the way in which the phenotype is shaped. Furthermore, an individual's phenotype is not fixed throughout that individual's life. The phenotypes of the developing foetus and infant and that of the elderly (or those in some other form of decline) are not the same as that of the adult and are typically overlooked. The changing phenotype of the pregnant female appears to have been completely overlooked. Furthermore, the phenotype is often represented as being something rather static. No organism lives the whole of its life at a constant, let alone an optimal, state. Males previously successful in winning the attention of females by some form of display or in gaining access to her by winning contests with other males ultimately fail to live up to their former successes. An organism's phenotype changes over time even though its genotype stays the same.

Furthermore, in the struggle for life, three separate aspects of the individual essential for ensuring survival were identified. These were the physical, experiential and behavioural states of the individual. Together, they form a survival triad. Together they can be used to locate the state of an individual in a phase space representing that individual's survival chances.

The fact that organisms can have an experiential state and that they are self-referential has largely gone unexplored in an evolutionary context. That there is an information flow within individual organisms and that this can reach the level of consciousness has not been something easy to access. Yet, based upon the nature of its interior world, each animal must make choices and decisions that affect its survival. There may be those species in which these choices and decisions are not intellectually reasoned in the human sense. Nevertheless, they are the product of something about the animal's internal experience. For a fuller understanding of the lived biology of the individuals that make up populations, factors such as these need to be explored further, drawing upon modern computational and modelling techniques as appropriate.

Dobzhansky suggested that nothing in biology makes sense except in the light of evolution. There is still much to be learnt about biology via the application of evolutionary ideas. There are areas that have not been explored thoroughly as yet. There are others that have been largely overlooked. A fuller understanding of individual organisms from an evolutionary perspective is still to be achieved. However, by doing so, it may be possible, in keeping with Dozhansky's suggestion, to make even more sense of biology.

17. Acknowledgement

I would like to thank Annette Lewis for her help in the preparation of the manuscript of this chapter.

18. References

Barker, D. J. P. (Ed.) (1992). Fetal and infant origins of adult disease. British Medical Journal, London

Bateson, P. & Martin, P. (1999) Design for a Life: How Behaviour Develops. Jonathan Cape, London

Boogerd, F.; Bruggeman, F.; Hormeyr, J.-H. & Westerhoff, H. (Eds.) (2007). Systems Biology - Philosophical Foundations. Elsevier, Amsterdam

Calcott, B. (2008). Assessing the fitness landscape revolution. Biology and Philosophy, Vol.23, No.5, pp. 639-657

Case, R. & Waterhouse, J. (1994). Human Physiology - Age, Stress, and the Environment. Oxford University Press, Oxford

Correns, C. (1900). G. Mendel's Regel über das Verhalten der Nachkommenschaft der Rassenbastarde, Berichte der deutschen botanischen Gesellschaft, Vol.18, pp. 158–168. (For an English translation by Leonie Kellen Piternick entitled, 'G. Mendel's Law Concerning the Behavior of Progeny of Varietal Hybrids', see C. Stern, & E.R. Sherwood, (Eds.), (1966), The Origin of Genetics: A Mendel Source Book 119-132, W.H Freeman and Company, New York)

Dawkins, R. (1989). The Extended Phenotype: The Long Reach of the Gene. Oxford University Press, Oxford

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

Darwin, C. (1859). On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. John Murray, London

Darwin, C. (1871). The Descent of Man, and Selection in Relation to Sex. John Murray, London

Dobzhansky, T. (1973). Nothing in biology makes sense except in the light of evolution. American Biology Teacher, Vol.35, pp. 125-129

Engel, C. (2003) Wild Health: How Animals Keep Themselves Well and What We Can Learn from Them. Pheonix, London

Fisher, R. A. (1930) The Genetical Theory of Natural Selection. The Clarendon Press, Oxford

Gould, S. J. (1974) Origin and Function of 'Bizarre' Structures - Antler Size and Skull Size in 'Irish Elk', Megaloceros giganteus. Evolution, Vol.28, No.2, pp. 191-220

Hamilton, W. D. (1963). The evolution of altruistic behavior. The American Naturalist, Vol.97, No.896, pp. 354-356

Hamilton, W. D. (1964a) The Genetical Evolution of Social Behaviour. I. Journal of Theoretical Biology, Vol.7, No.1, pp. 1-16

Hamilton, W. D. (1964b) The Genetical Evolution of Social Behaviour. II. Journal of Theoretical Biology, Vol.7, No.1, pp. 17-52

Henig, R. M. (2009) The Monk in the Garden: The Lost and Found Genius of Gregor Mendel, the Father of Modern Genetics. Houghton Mifflin, Boston and New York

Hunter, C. & Clegg E. J. (1973a). Changes in body weight of the growing and adult mouse in response to hypoxic stress. Journal of Anatomy, Vol.114, No.2, pp. 185-199

Hunter C, & Clegg E. J. (1973b) Changes in skeletal proportions of the rat in response to hypoxic stress. Journal of Anatomy, Vol.114, No.2, pp. 201-19

Johannsen W. (1911). The genotype conception of heredity. The American Naturalist, Vol.45, pp. 129-159

Kimura, M. (1968). Evolutionary rate at the molecular level. Nature, Vol.217 No.5129, pp. 624–626

Kitano, H. (2002). Systems Biology: A Brief Overview. Science, Vol.295, (1st March), pp. 1662-1664

Komlos, J. (1998). Shrinking in a Growing Economy? The Mystery of Physical Stature during the Industrial Revolution, Journal of Economic History, Vol.58, No.3, pp. 779-802

Lewis, S. (2008). Evolution At The Intersection Of Biology And Medicine, In: Evolutionary Medicine and Health - New Perspectives, W.R. Trevathan, E.O. Smith, & J.J. McKenna, (Eds.), 399-415, Oxford University Press. New York

Lewis, S. (2011). Conceptual Models of the Human Organism: Towards a New Biomedical Understanding of the Individual, In: Biomedical Engineering, Trends, Research and Technologies. M.A. Komorowska, & S. Olsztynska-Janus, (Eds.), InTech, Rijeka, Croatia

Maynard Smith, J. (1964). Group Selection and Kin Selection. Nature, Vol.201, No.4924, pp. 1145-1147

Maynard Smith, J. (1989) Evolutionary Genetics, Oxford University Press, Oxford

McHugh, S. & Vallis, T. (Eds.), (1986). Illness behaviour, a multidisciplinary model, Plenum Press, New York

Moen, R. A.; Pastor, J. & Cohen, Y. (1999). Antler growth and extinction of Irish elk. Evolutionary Ecology Research, Vol.1, No. 2, pp. 235-249

Nesse, R. (2001a). How is Darwinian medicine useful? Western Journal of Medicine, Vol.174, pp. 358-360

Nesse, R. (2001b). Medicine's missing basic science. The New Physician, (December 2001), pp. 8-10

Nesse, R. (October 2011). What is Darwinian Medicine?, In: Evolutionary Medicine (Website), 01.10.11, Available from

http://sites.google.com/site/evolutionarymedicine/home/texts/text1

Nesse, R.; Stearns, S. & Omenn, G. (2006). Medicine Needs Evolution. Science, Vol.311, pp. 1071-1073

Nesse, R. & Williams, G. (1994). Why We Get Sick - The new science of Darwinian medicine. Times Books, New York

Nesse, R. & Williams, G. (1995). Evolution and Healing - The new science of Darwinian medicine. Weidenfeld and Nicolson, London

Nesse, R. & Williams, G. (1997). Evolutionary biology in the medical curriculum - what every physician should know. Bioscience, Vol.47, pp. 664-666

Petrie, M. (1994). Improved growth and survival of offspring of peacocks with more elaborate trains. Nature, Vol.371, No.6498, pp. 598-599

Pigliucci, M. (2008). Sewall Wright’s adaptive landscapes: 1932 vs. 1988. Biology and Philosophy, Vol.23, No.5, pp. 591-603

Provine, W. (1986). Sewell Wright and Evolutionary Biology. University of Chicago Press, Chicago

Refinetti, R. (2005). Time for sex: nycthemeral distribution of human sexual behavior. Journal of Circadian Rhythms, Vol.3, No.1, p. 4

Rose, H. & Rose, S. (Eds.). (2001). Alas Poor Darwin - Arguments against Evolutionary Psychology. Vintage, London

Shin, T.; Kraemer, D.; Pryor, J.; Liu, L.; Rugila, J.; Howe, L.; Buck, S.; Murphy, K.; Lyons, L. & Westhusin, M. (2002) A cat cloned by nuclear transplantation, Nature, Vol.415, (21 February 2002), p859

Simpson, G. (1944). Tempo and Mode in Evolution. Columbia University Press, New York

Simpson, G. (1953). The Major Features of Evolution. Columbia University Press, New York

Skipper, R. Jr, (2004). The heuristic role of Sewall Wright's 1932 adaptive landscape diagram. Philosophy of Science, Vol.71, pp. 1176–1188

Smith, B. & Kumar, A. (2005). On the proper treatment of pathologies in biomedical ontologies, Proceedings of Bio-Ontologies Workshop, Detroit, (24 June 2005)

Available from

http://bio-ontologies.org.uk/2005/download/ISMB1.doc

Spencer, H. (1864). The Principles of Biology. Vol 1. Williams & Norgate, London.

Watson, J. D. & Crick, F. H. (1953). Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature, Vol.171, No.4356, pp. 737–738.

Weismann, A. (1892). Das Keimplasma: eine Theorie der Vererbung, Fischer, Jena (Translated as The Germ-Plasm: A theory of heredity (trans. W.N. Parker & H. Rönnfeldt), Charles Scribner's Sons, New York, 1893)

Williams, G., & Nesse, R. (1991). The dawn of Darwinian medicine. The Quarterly Review of Biology, Vol.66, pp. 1-22

Wright, S. (1929). The evolution of dominance. The American Naturalist, Vol.63, No.689, pp. 556–61

Wright, S. (1932). The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proceedings of the 6th International Congress on Genetics, Vol.1, pp. 356-366

Wright, S. (1980). Genic and organismic selection. Evolution, Vol.34, Vol.5, pp. 825-843

Wright, S. (1988). Surfaces of Selective Value Revisited. The American Naturalist, Vol.131, pp. 115-123