Evolution ‘on purpose’: how behaviour has shaped the evolutionary process



The idea that behaviour has played an important role in evolution has had its ups and downs over the past two centuries. Now it appears to be up once again. Lamarck can claim priority for this insight, along with Darwin's more guarded view. However, there followed a long ‘dark-age’, which began with Weismann's mutation theory and spanned the gene-centred era that followed during most of the 20th Century, although it was punctuated by various contrarians, from Baldwin's ‘Organic Selection theory’ to Simpson's ‘Baldwin effect’, Mayr's ‘Pacemaker’ model, and Waddington's ‘genetic assimilation’, amongst others. Nowadays, even as we are reading genomes and using this information to illuminate biological causation and decipher evolutionary patterns, behavioural processes are more fully appreciated, with ‘multilevel selection theory’ providing a more ecumenical, multicausal model of evolutionary change. This has been accompanied by a flood of research on how behavioural influences contribute to the ongoing evolutionary process, from research on phenotypic plasticity to niche construction theory and gene–culture co-evolution theory. However, the theoretical implications of this paradigm shift still have not been fully integrated into our current thinking about evolution. Behaviour has a purpose (teleonomy); it is ends-directed. Living organisms are not passive objects of ‘chance and necessity’ (as Jacques Monod put it). Nor is the currently popular concept of phenotypic plasticity sufficient. Organisms are active participants in the evolutionary process (cybernetic systems) and have played a major causal role in determining its direction. It could be called ‘constrained purposiveness’, and one of the important themes in evolution, culminating in humankind, has been the ‘progressive’ evolution of self-determination (intelligence) and its ever-expanding potency. I call this agency ‘Teleonomic Selection’. In a very real sense, our species invented itself. For better and worse, the course of evolution is increasingly being shaped by the ‘Sorcerer's Apprentice’. Monod's mantra needs to be updated. Evolution is a process that combines ‘chance, necessity, teleonomy and selection’. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 242–260.

The Origin of An Idea

The idea that evolution is a ‘purposeful’, teleological process has been anathema to evolutionary biologists ever since Darwin. Indeed, the fundamental distinction between a contingent, historical, ‘trial-and-success’ process and a deterministic directional process, whether divinely sanctioned or as the result of some hidden natural force or ‘law’, lies at the very heart of the great divide between scientific and religious world views. The late Stephen Jay Gould, a leading palaeontologist of the 20th Century, was particularly eloquent about it. He firmly rejected the idea of evolutionary ‘progress’ and proposed that evolution has been more like a ‘drunkard's walk’ (Gould, 1996).

Nevertheless, there can be no denying the evidence of an overall trend in evolution over time toward greater complexity, along with greater power to shape the evolutionary process in purposeful ways, as highlighted especially in work on ‘phenotypic plasticity’ (West-Eberhard, 1989, 2003, 2005; Pigliucci, 2001), ‘niche construction theory’ (Laland, Odling-Smee & Feldman, 2001; Odling-Smee, Laland & Feldman, 2003), ‘gene–culture coevolution theory’ (Feldman & Laland, 1996; Boyd & Richerson, 2005; Richerson & Boyd, 2005, 2010), and ‘natural genetic engineering’ (Shapiro, 1991, 1992, 2012). This aspect of the evolutionary process is best exemplified by the evolution of Homo sapiens.

Thus, there remains a deep conundrum in evolutionary theory. How did purposefulness (what the distinguished 20th Century biologist Theodosius Dobzhansky called an ‘internal teleology’) evolve, and how did this contribute to the enormous biological complexity (and diversity) that we can observe today?

One of the earliest ‘modern’ theorists to propose the idea of an inherent evolutionary trend toward complexity was the famed 18th and early 19th Century naturalist Jean Baptiste de Lamarck (1984/1809) (although the basic idea can be traced back at least to Aristotle). In his Zoological Philosophy, Lamarck spoke of an inherent energetic force (a ‘power of life’) that presaged Herbert Spencer's grandiose, energy-centred ‘law of evolution’ (Spencer, 1892/1852), as well as the aspirations of some modern-day physicists and complexity theorists (Kauffman, 1993, 1995, 2000). Darwin was deeply opposed to this formulation, although he did recognize Lamarck's role in championing the then unpopular view that life on Earth had gradually evolved.

Lamarck is best-known, even infamous, for his thesis that the course of evolution has also been shaped by ‘habits acquired by conditions’ (i.e. the direct inheritance of traits developed during the lifetime of an individual organism). This idea did not originate with Lamarck. It was ‘in the air’ at the time, and Lamarck (similarly to Darwin) could only guess what the precise mechanism of inheritance might be. He lived long before the discovery of genes and the genetic code. The long necks of giraffes served as an illustration; Lamarck proposed that this distinctive animal trait arose because ancestral giraffes had progressively stretched their necks over many generations to reach the leaves in the tops of acacia trees, and that the changes were then passed on to their offspring (Cannon, 1955, 1959; Gissis & Jablonka, 2011).

Darwin was scornful of this idea in his earlier years. ‘Heaven forfend me from Lamarck's nonsense’, he wrote to a friend in 1844. But, in The Origin of Species, Darwin displayed his usual scientific caution by not ruling out the possibility that environmental influences and ‘the use and disuse of parts’ (as he put it) could be one source of biological variation and adaptation in nature. He even cited some possible evidence in its favour (Darwin, 1968/1859: 175). Yet, for obvious reasons, Darwin considered Lamarckian influences to be a minor subsidiary to natural selection.

The rise of the science of genetics at the turn of the 20th Century put a conclusive end to Lamarck's theory of acquired characters. In a classic (if gruesome) experiment, the pioneer geneticist August Weismann (1904) cut off the tails of 20 successive generations of mice without, of course, producing a tailless strain. Other evidence against Lamarck's thesis could be found in the practices of farmers and pet breeders, who routinely dock tails, notch ears, castrate males, spay females, and so on. There are also such human customs as circumcision, pierced ears and noses, shaved heads, and various forms of deliberate mutilation, none of which is heritable.

Unfortunately, in the process of rejecting the Lamarckian view of inheritance, the baby got thrown out with the bath water; the role of behaviour as an important causal factor in evolutionary change was also summarily rejected. Weismann's claim that random mutations are the underlying source of creativity in evolution became one of the cornerstones of the nascent science of genetics and, ultimately, of a gene-centered evolutionary theory. For a time Weismann's ‘mutation theory’ even eclipsed Darwinism. However, in the 1930s, a new theoretical synthesis was achieved. It was recognized that, if mutations (and the process of ‘recombination’ in sexual reproduction) are responsible for generating biological novelties, they must subsequently be ‘tested’ in the environment by natural selection. This perspective is captured by psychologist Donald Campbell's (1974) popular slogan ‘blind variation and selective retention’. The prominent 20th Century evolutionary biologist Ernst Mayr (1965) characterized it as a ‘two-step, tandem process’.

Although this mechanistic, gene-centred paradigm appealed to a young science that aspired to mimic the law-governed rigour of the then reigning ‘queen’ of the sciences (physics), it also provided an insufficient account of the dynamics of evolution because it left the organism out of the equation. The ‘phenotype’ was treated as a passive object, a ‘black box’ whose fate is determined by the impersonal forces of genes and the environment. Patrick Bateson (1988) has called it the ‘billiard ball’ theory of evolution. However, living systems are more than billiard balls, or ‘robot vehicles’ as some theorists have suggested. They are in fact active participants in the evolutionary process. Although Lamarck may have guessed wrong about the machinery of inheritance, he deserves credit for recognizing the importance of the organism and its behaviour as a distinct causal agency in evolutionary change.

Lamarck no less than Darwin appreciated that functional adaptation to the environment is a problem for any organism. However, the environment is not fixed, Lamarck observed, and, if circumstances (circonstances) change, an animal must somehow accommodate itself or it will not survive. Changes in the environment over the course of time can thus be expected to give rise to new needs (besoins) that in turn will stimulate the adoption of new ‘habits’. Furthermore, asserted Lamarck, changes in habits come first and structural changes may follow. He wrote: ‘It is not the organs … of an animal's body that have given rise to its special habits and faculties; but it is, on the contrary, its habits, mode of life and environment that have in the course of time controlled the shape of its body, the number and state of its organs and, lastly, the faculties which it possesses’ (Lamarck 1984/1809: 114).1

Darwin also appreciated the role of behaviour in evolutionary change, although his view of its relative importance was more guarded. He wrote: ‘It is difficult to tell, and immaterial for us, whether habits generally change first and structure afterwards; or whether slight modifications of structure lead to changed habits; both probably often change almost simultaneously’ (Darwin, 1968/1859: 215).

Organic Selection and Beyond

Many of Darwin's successors were not so ecumenical but, at the turn of the 20th Century, a movement developed concurrently among several British and American scientists who, in effect, Darwinized Lamarckism and assigned to behaviour a more prominent role in evolution. Although their perspectives differed somewhat, their views were generally lumped together under psychologist James Mark Baldwin's term ‘Organic Selection’ (Baldwin, 1896a, b, c, 1902; also Lloyd Morgan, 1891, 1896a, b, 1908/1900; Osborn, 1896a, b, 1897).

The basic claim of Organic Selection theory was that, in the course of evolution, the first step in producing systematic biological changes might well be a change in behaviour, especially among the more ‘plastic’ species, a term coined by Lloyd Morgan (1896a) and later adopted by Baldwin. When an animal is in some way able to modify its behaviour so that it can ‘select’ a new habitat, or a new mode of adaptation, after a number of generations the change might precipitate congenital changes ‘in the same direction’ that would undergird and perfect the new adaptation. This would occur not because the changes are somehow stamped into the offspring but because the new environment creates a ‘screen’ that would selectively favour individuals with the relevant ‘somatic variations’ (Baldwin, 1896c).

Lamarck's giraffes are a possible case in point. Naturally occurring variations in the neck lengths of ancestral Giraffidae most likely became adaptively significant when these animals acquired, perhaps through trial-and-error, a new ‘habit’ (eating Acacia leaves) as a way of surviving in the relatively desiccated environment of the African savanna. We cannot know for certain that this was the case, but some suggestive evidence can be found in a related species of short-necked giraffe, the okapi. Significantly, okapi occupy woodland environments and, as expected, have very different feeding habits.

From a modern perspective, Baldwin's Organic Selection theory was crudely formulated. It was worded ambiguously; it was not at first firmly Darwinian; it displayed a deficient understanding of natural selection; it was based on a rudimentary pain-pleasure model of behaviour; it was hypothetical; and it did not lend itself to being ‘bench-tested’ in the way that genetically-determined traits can be manipulated in laboratory strains of Drosophila (fruit flies). With the emergence of the science of genetics, the Organic Selection idea, and Lamarckism, went into a total eclipse.

However, its theoretical demise proved to be temporary. In the early 1950s, a modest effort to rehabilitate Organic Selection was undertaken by palaeontologist George Gaylord Simpson (1953), who renamed it the ‘Baldwin effect’. However, Simpson defined it very narrowly and treated it as a subsidiary phenomenon. ‘It does not, however, seem to require any modification of the opinion that the directive force [his emphasis] in adaptation, by the Baldwin effect or in any other particular way, is natural selection’ (Simpson, 1953: 116). Simpson did not, of course, mention Lamarck.2

Meanwhile, an independent-minded British embryologist and geneticist, Conrad Hal Waddington, challenged the mainstream viewpoint when he produced experimental evidence (published in Nature but nonetheless downplayed by other geneticists) for a Darwinized version of Lamarckian inheritance that he called ‘genetic assimilation’ (Waddington, 1942, 1952). Using the geneticists’ favourite experimental species, fruit flies (because they are low-cost, reproduce rapidly and have many single-gene traits that can be altered readily in selection experiments), Waddington showed that certain developmentally-influenced behavioural characters, such as sensitivity to various environmental stimuli, could be enhanced through differential selection to the point where the traits would appear ‘spontaneously’, even in the absence of the stimuli.

Waddington also became a vocal critic of the gene-centred view of evolution. As he pointed out, ‘It is the animal's behaviour which to a considerable extent determines the nature of the environment to which it will submit itself and the character of the selective forces with which it will consent to wrestle. This “feedback” or circularity in a relation between an animal and its environment is rather generally neglected in present-day evolutionary theorizing’ (reprinted in Waddington, 1975: 170).

However, a major (mainstream) reconsideration of the issue occurred in the late 1950s, when the American Psychological Association and the then-new Society for the Study of Evolution jointly organized a set of conferences that resulted in the important edited volume called Behavior and Evolution (Roe & Simpson, 1958). This often-cited work contained a mother-lode of tantalizing ideas: there is the suggestion that adaptive radiations, an important aspect of evolutionary change, might be ‘fundamentally behavioral in nature’ (Simpson), that behaviour might often serve as an isolating mechanism in the formation of new species (Spieth), that all organisms, inclusive of their behaviour, are ‘teleonomic’ (purposeful) systems (Pittendrigh), and that, in the process of evolutionary change, new behaviours may appear first and genetic changes may follow (Mayr).

Mayr elaborated on his views 2 years later in a major article that became a theoretical landmark, ‘The Emergence of Evolutionary Novelties’, in which he characterized behavioural changes as the ‘pacemaker’ of evolution (Mayr, 1960; see also Mayr, 1974). Needless to say, none of this was associated with the discredited Lamarck.

Behaviour As a ‘Pacemaker’ of Evolution

The number of publications highlighting the role of learning and behaviour in evolution rose to a crescendo in the late 1950s and 1960s, with the appearance of such important books as W. H. Thorpe's (1956) Learning and Instinct in Animals; C. H. Waddington's (1957, 1961) The Strategy of the Genes and The Nature of Life; Alistair Hardy's (1965) The Living Stream; Lancelot Law Whyte's (1965) Internal Factors in Evolution; Robert A. Hinde's (1966) Animal Behaviour: A Synthesis of Ethology and Comparative Psychology; and Arthur Koestler's (1967) The Ghost in the Machine.3 Many of the examples of novel behaviours that were described in these and other works of that era have become legendary: the blue tits that learned to remove milk bottle caps (Gould & Gould, 1994; Byrne, 1995); problem solving behaviours in chimpanzees (Köhler, 1925) and honeybees (von Frisch, 1967); the inventive Japanese macaque Imo (Kawai, 1965); and the chimpanzee, Mike, who learned to use a steel drum to terrorize his mates (Goodall, 1986), amongst others.

In the half century since the 1960s, the research literature on learning and innovation in living organisms (from ‘smart bacteria’ to human-tutored apes and playful dolphins) has grown to cataract proportions. (Indeed, there is now so much of it that some excellent earlier work is being overlooked and forgotten.) The examples are almost endless: worms, fruit flies, honeybees, guppies, stickleback fish, ravens, various song birds, hens, rats, gorillas, chimpanzees, elephants, dolphins, whales, and many others (Eytan Avital & Eva Jablonka, 2000, list well over 200 different species in the index to their book on Animal Traditions).

We now know that primitive Escherichia coli bacteria, Drosophila flies, ants, bees, flatworms, laboratory mice, pigeons, guppies, cuttlefish, octopuses, dolphins, gorillas, and chimpanzees, among many other species, can learn novel responses to novel conditions via ‘classical’ and ‘operant’ conditioning. (One cynic has pointed out that behavioural scientists have only confirmed what pet lovers and circus animal trainers have known for centuries.)

Our respect for the ‘cognitive’ abilities of various animals also continues to grow. Innumerable studies have documented that many species are capable of sophisticated cost–benefit calculations, sometimes involving several variables, including perceived risks, energetic costs, time expenditures, nutrient quality, resource alternatives, relative abundance, and more. Animals are constantly required to make ‘decisions’ about habitats, foraging, food options, travel routes, nest sites, even mates.4 Many of these decisions are under tight genetic control, with ‘pre-programmed’ selection criteria. However, many more are also, at least in part, the product of past experience, trial-and-error learning, observation and even, perhaps, some insight learning. One classic illustration is Bernd Heinrich's experiments in which naïve ravens quickly learned how to pull up ‘fishing lines’ with the use of their beaks and claws to capture the food rewards that were attached (Heinrich, 1995). Heinrich's (1999) book, The Mind of the Raven, provides extensive evidence for the mental abilities of these remarkable birds.

Indeed, biologists Simon Gilroy & Anthony Trewavas (2001) have found that even plants make ‘decisions’. In the marine alga Fucus, for example, at least 17 environmental conditions can be ‘sensed’, and the information that it collects is then either summed or integrated synergistically as appropriate. Gilroy & Trewavas conclude: ‘What is required of plant-cell signal-transduction studies … is to account for “intelligent” decision-making; computation of the right choice among close alternatives’.

Especially important theoretically are the many forms of social learning through ‘stimulus enhancement’, ‘contagion effects’, ‘emulation’, and even some ‘teaching’. Social learning has been documented in many species of animals, from rats to bats, to lions and elephants, as well as some birds and fishes and, of course, domestic dogs. For example, red-wing blackbirds, which readily colonize new habitats, are especially prone to acquire new food habits (or food aversions) from watching other birds (Weigl & Hanson, 1980). Pigeons can learn specific food-getting skills from other pigeons (Palameta & LeFebvre, 1985). Domestic cats, when denied the ability to observe conspecifics, will learn certain tasks much more slowly or not at all (John et al., 1968). In a controlled laboratory study, naive ground squirrels (Tamiasciurus hudsonicus) that were allowed to observe an experienced squirrel feed on hickory nuts were able to learn the same trick in half the time it took for unenlightened animals (Byrne, 1995: 58).

True ‘imitation’ (including the learning of motor skills) has also been observed in (amongst others) gorillas (peeling wild celery to get at the pith), rats (pressing a joy stick for food rewards), African grey parrots (vocalizations and gestures), chimpanzees (nut-cracking with an anvil and a stone or wooden hammer), and bottlenose dolphins (many behaviours, including grooming, sleeping postures, even mimicking the divers that scrape the observation windows of their pools, down to the sounds made by the divers’ breathing apparatus).

Not surprisingly, the most potent cognitive skills have been found in social mammals, especially the great apes. They display intentional behaviour, planning, social coordination, understanding of cause and effect, anticipation, generalization, and even deception. Primatologists Richard Byrne and Andrew Whiten, in their two important edited volumes on the subject, refer to it as ‘Machiavellian intelligence’ (Byrne & Whiten, 1988; Gibson & Ingold, 1993; Whiten & Byrne, 1997). Social learning provides a powerful means (which humankind has greatly enhanced) for accumulating, diffusing and perpetuating novel adaptations without waiting for slower-acting genetic changes to occur.

Tool-use is an especially significant and widespread category of adaptive behaviour in the natural world (from insects to insectivores and omnivores) and it is utilized for a wide variety of purposes. As Edward O. Wilson (1975) pointed out in his comprehensive survey and synthesis, Sociobiology, tools provide a means for quantum jumps in behavioural invention, as well as in the ability of living organisms to manipulate their environments. Tool-use results in otherwise unattainable behavioural effects (synergies) (Wilson, 1975: 172; Beck, 1980; McGrew, 1992).

Chimpanzees are particularly impressive tool users. They frequently use saplings as whips and clubs; they throw sticks, stones, and clumps of vegetation with a clearly hostile intent (but rather poor aim); they insert small sticks, twigs, and grasses into ant and termite holes to ‘fish’ for booty; they use sticks as pry bars, hammers, olfactory aids (to sniff out the contents of enclosed spaces), and even as toothpicks; they also use stones as anvils and hammers (for breaking open the proverbial tough nuts); and they use leaves for various purposes: as sponges (to obtain and hold drinking water), as umbrellas (large banana leaves are very effective), and for wiping themselves in various ways (including chimpanzee equivalents of toilet paper and sanitary napkins) (Wilson, 1975; Beck, 1980; McGrew, 1992; Wrangham et al., 1994).

Finally, it is important to take note of the role of ‘culture’ and cultural transmission in evolutionary change. The debate about culture in other species, such as chimpanzees, may still be unresolved, although there can be no doubt that behavioural and cultural evolution played an important role in human evolution (Wills, 1993; Foley, 1995; Diamond, 1997; Klein, 1999; Wolpoff, 1999; Wrangham, 1999, 2001; Ehrlich, 2000; Klein & Edgar, 2002; Corning, 2003, 2012; Boyd & Richerson, 2005, 2009; Richerson & Boyd, 2005, 2010; Richerson, Boyd & Henrich, 2010; Foley & Gamble, 2011; Laland, Odling-Smee & Myles, 2011). As biologist Jonathan Kingdon (1993) summed up in the title of his insightful book on this subject, we are the Self-Made Man.

Biologist Lynn Margulis and co-author Dorion Sagan (Margulis & Sagan, 1995), in their book What is Life?, characterized evolution as the ‘sentient symphony’. What is most significant about the behaviour of living organisms, they claimed, is their ability to make choices. (For the record, Waddington mounted a very similar argument back in the 1950s, along with Lloyd Morgan in his 1896 book.) Margulis and Sagan, allowing themselves a bit of poetic license, wrote: ‘At even the most primordial level, living seems to entail sensation, choosing, mind’ (Margulis & Sagan, 1995: 180).

This view is convincingly supported in microbiologist James Shapiro's (2012) book, Evolution: A View from the 21st Century. He notes that we are currently in the midst of ‘a deep rethinking of basic evolutionary concepts’ (Shapiro, 2012: xvii). There is a paradigm shift underway from an atomistic, reductionist, gene-centred, mechanical model to a systems perspective in which ‘purposeful’ actions and informational processes are recognized as fundamental properties of living systems at all levels. These properties play an important role in what Shapiro refers to as ‘natural genetic engineering’. As he emphasizes, ‘The capacity of living organisms to alter their own heredity is undeniable. Our current ideas about evolution have to incorporate this basic fact of life’ (Shapiro, 2012: 2).5

What is Natural Selection?

Lamarck, it seems, was on the right track regarding the fundamentally important role of behaviour in evolution. The evidence would appear to be overwhelming. Yet there is still some reluctance to incorporate this theoretical insight into the core explanans of evolutionary biology. Indeed, the standard definition of evolution has always tended to be narrow, gene-centred, and circular. Evolution in the mainstream paradigm is defined as ‘a change in gene frequencies’ in a given ‘deme’, or breeding population, and natural selection is defined as a ‘mechanism’ that produces changes in gene frequencies. As the biologist John H. Campbell put it in a review: ‘Changes in the frequencies of alleles by natural selection are evolution’ (Campbell, 1994: 86). By implication, it follows that mutations and related molecular-level changes (subject to the ‘approval’ of natural selection) are the only important sources of novelty in evolution.

However, natural selection is not a ‘mechanism’. It does not do anything; nothing is ever actively selected (although sexual selection and artificial selection are special cases). Nor can the sources of causation be localized either within an organism or externally in its natural environment. Indeed, the term natural selection, as Darwin utilized it, is a metaphor (i.e. a label that identifies an aspect of the evolutionary process). The core assumption of evolutionary biology is that life is fundamentally a ‘survival enterprise’ that is always contingent. Thus, natural selection is a kind of umbrella term that refers to whatever functionally-significant factors are responsible in a given context for causing differential survival and reproduction. Properly conceptualized, these ‘factors’ are intensely interactional and relational; they are defined by both the organism(s) and their environment(s). [A textbook illustration is the classic study of ‘industrial melanism’ in the peppered moth, Biston betularia by Kettlewell (1955, 1973), which has recently been reconfirmed by geneticist Mike Majerus; see Hurley & Montgomery (2009)].

Another way of stating it is that the standard definition equates natural selection and evolution with genetic changes, rather than viewing evolution more expansively as a multilevelled process in which genes, other molecular factors, genomes, developmental (‘epigenetic’) influences, mature phenotypes, and the natural environment interact with one another and evolve together in a dynamic relationship of mutual and reciprocal causation, including (in the current jargon) ‘upward’ causation, ‘downward’ causation, and even ‘horizontal’ causation (e.g. in predator–prey interactions or among symbionts). The emergence of ‘multilevel selection theory’ in biology during the past two decades has been an important step in the right direction. (See the special issue of the American Naturalist regarding this development, especially the Introduction by David Sloan Wilson, 1997; see also Okasha, 2006; Traulsen & Nowak, 2006.).

Thus, many things, at many different levels, may be responsible for bringing about changes in an organism–environment relationship, and differential survival. It could be a functionally-significant mutation, a chromosomal transposition, a change in the physical environment that affects development, a change in one species that affects another species, or it could be a change in behaviour that results in a new organism-environment relationship. Indeed, a whole sequence of changes may ripple through a pattern of relationships. For example, a climate change might alter the ecology, prompting a behavioural shift to a new habitat, which might encourage an alteration in nutritional habits, thus precipitating changes in the interactions among different species, ultimately resulting in the differential survival and reproduction of alternative morphological characters and the genes that support them. An in vivo illustration of this causal dynamic can be found in the long-running research programme in the Galápagos Islands among ‘Darwin's finches’ (Grant & Grant, 1979, 1989, 1993; Weiner, 1994; Grant & Grant, 2002).

Teleonomy in Evolution

Despite all the developments described above, there is still reluctance among evolutionary biologists to recognize and incorporate into the core of evolutionary theory the fundamental ‘purposiveness’ and partial-autonomy of living systems (although it should properly be called ‘constrained purposiveness’). Physics, long the model science, traditionally pursued the search for impersonal, mechanistic ‘laws’ that are applicable anywhere and any time. Teleology had no place in this enterprise, needless to say, and biology slavishly followed suit in earlier generations. However, in the 1960s and 1970s, a number of voices were raised against this ultimately deficient view of how living systems work (e.g. Monod, 1971). The case was argued most eloquently, perhaps, by Theodosius Dobzhansky:

Purposefulness, or teleology, does not exist in nonliving nature. It is universal in the living world. It would make no sense to talk of the purposiveness or adaptation of stars, mountains, or the laws of physics. Adaptedness of living beings is too obvious to be overlooked … Living beings have an internal, or natural, teleology. Organisms, from the smallest bacterium to man, arise from similar organisms by ordered growth and development. Their internal teleology has accumulated in the history of their lineage. On the assumption that all existing life is derived from one primordial ancestor, the internal teleology of an organism is the outcome of approximately three and a half billion years of organic evolution … Internal teleology is not a static property of life. Its advances and recessions can be observed, sometimes induced experimentally, and analyzed scientifically like other biological phenomena (in Dobzhansky et al., 1977: 95–96).

The term that is most often used by biologists these days to characterize the internal teleology of living organisms is ‘teleonomy’. Originally coined by biologist Colin Pittendrigh (1958) in connection with the 1958 conference on behaviour in evolution (as noted earlier), the term connotes the fact that the purposefulness found in nature is a product of evolution and not of a grand design. Teleonomy in living systems is today accepted without question. Yet few theorists take the next step and draw out the implications for evolutionary theory. Teleonomy puts living organisms into a unique category. An organism cannot be reduced to the laws of physics, or be derived from those laws, because its properties (inclusive of its structure, its behaviour and its historical trajectory) cannot be predicted from those laws. For example, the laws of physics are silent about the phenomenon of ‘feedback’, a fundamental (informational) aspect of all living systems.6

Many theorists skirt this issue by treating organisms as mere vessels (rudderless rafts, not motor boats) that are controlled by ‘exogenous’ factors: genes and the environment. For example, Edward O. Wilson (1975) speaks of behaviour as something that is ‘induced’ by environmental forces and ‘epigenetic rules’. The genetic ‘leash’ may be long, in Wilson's metaphor, but it is still a tight leash; see also West-Eberhard (2003). Other theorists describe evolution as a process in which organisms ‘track environmental changes’. Geneticist Richard Lewontin (1978), in a much-cited essay on the subject that he might word differently today, asserted that ‘the external world sets certain “problems” that organisms need to “solve”, and that evolution by means of natural selection is the mechanism for creating those solutions’ (Lewontin, 1978: 213).

In his celebrated book Chance and Necessity, the Nobel Prize-winning geneticist Jacques Monod (1971) characterized evolution as a process that is governed by two great influences, ‘chance and necessity’.7 In Monod's formulation, the teleonomy of living systems is an epiphenomenon of random mutations and the ‘lock-in’ of natural selection. His focus was the evolved teleonomy found in the genome. Although he did acknowledge the role of behaviour in evolution, he treated it as a bit player, or a spear carrier, in the process; it did not have a starring role, except in human evolution. In the final peroration of his book, Monod concluded: ‘Man knows at last that he is alone in the universe's unfeeling immensity, out of which he emerged only by chance’ (Monod, 1971: 180).

In the tradition of Lamarck and a long line of dissenters from this constricted vision of evolution, I disagree. The purposiveness of living organisms represents a major (emergent) causal agency in evolution. Whether or not there is a purposiveness or directionality in the process as a whole is beside the point. That is a question best left to the theologians and the complexity theorists. From an evolutionary perspective, the natural world displays ‘the piling up of little purposes’, as Margulis & Sagan (1995) put it.

Teleonomy is found at every level in living systems. As Monod himself pointed out, it is embedded in the genome of every living organism and plays itself out in the process of morphogenesis and development. It is also evident in the phenotype (both in its morphology and its behaviour) and it imposes many functional imperatives and constraints on how an organism goes about earning its living.

As noted earlier, there is much greater appreciation today for the role of developmental and life-history influences in shaping the phenotypes of various species (from the hormonal state of the mother to ambient weather conditions in the animal's environment). Terms such as ‘phenotypic plasticity’, ‘norms of reaction’, and ‘reaction ranges’ are commonplace, and there are frequent references to the complex interplay of various factors via ‘epigenetic cascades’, ‘ontogenetic networks’, and similar terms; see especially West-Eberhard (1989, 2003, 2005); see also Pigliucci (2001); Stamps (1991); Stamps & Groothuis (2010); Stamps, Krishnan & Willits (2009); Robinson (2000); Robinson & Dukas (1999); Robinson, Januszkiewicz & Koblitz (2008); Dukas (1998, 2008, 2010); ten Cate & Rowe (2007); Verzijden & ten Cate (2007).

Indeed, behavioural innovations, however they may occur, are beginning to look like the explanation for some of the outstanding puzzles in the natural world. One notable example is the extraordinary diversity of cichlid fish in African lakes, such as Lake Victoria, which is of recent origin. It is now assumed that a highly malleable morphological trait in these creatures, namely their jaw structure, interacted with a great profusion of new food ‘habits’ (specializations on different resources) to accelerate the evolutionary process (Stiassny & Meyer, 1999). Similarly, the approximately 110 species of anole lizards in the Greater Antilles islands correlate well with the diversity of the ‘niches’ that they occupy on different islands: grass, tree branches, tree trunks, etc. Here again, a high degree of phenotypic flexibility may have contributed (Foster, 1999; Losos, 2001).

Nonetheless, many proponents of phenotypic plasticity still adhere closely to the ‘mainstream’ evolutionary paradigm. Thus, Mary Jane West-Eberhard in her comprehensive 2003 volume on the subject, defines phenotypic plasticity as ‘the ability of an organism to react to an internal or external environmental input with a change in form, state, movement or rate of activity’. Furthermore, ‘Phenotypic innovation depends on developmental innovation … I argue that the most important initiator of evolutionary novelties is environmental induction’ (West-Eberhard, 2003: 33, 144). In other words, the organism is not an autonomous actor but a reactor.

This formulation is insufficient, in my view. In the jargon of decision science, living beings are value-driven decision systems. Much of the research relating to the teleonomic model of behaviour these days goes under the headings of ‘behavioural ecology’ and ‘cognitive ethology’, and there has been a lively debate about the nature of animal intelligence and whether or not animals have ‘minds’. These issues aside, the common thread is the assumption that animals are ‘intentional systems’ (in philosopher Daniel Dennett's term).8 It is taken as a given that there is at least a degree of autonomy (i.e. some degrees of freedom) in the shaping of animal choices.

‘Downward Causation’

One other related concept should be briefly mentioned. Much of the purposiveness in living systems can be said to be a product of ‘upward causation’ (i.e. the expression of the genes and the genome). However, much also entails ‘downward causation’, from the whole to the parts. Here, Lamarck's insight, as properly modernized and Darwinized, comes into its own.

Although the term ‘downward causation’ is often associated with the psychologist and evolutionary epistemologist Donald T. Campbell (1974), who may have developed it independently, the term was actually coined years earlier by the well-known psychobiologist Roger Sperry (1969, 1991) with reference to higher-level control functions in the human brain. Sperry was fond of using the metaphor of a wheel rolling down hill; its rim, its hub, all of its spokes, indeed, all of its atoms are compelled to go along for the ride. (A similar concept, termed ‘supervenience’, was put forward in the early years of the 20th Century by the proponents of ‘Emergent Evolution’, most notably Conwy Lloyd Morgan, 1923, 1926, 1933.)

From an evolutionary perspective, downward causation/supervenience refers especially to purposeful activities at higher levels of organization in living systems (the phenotype) that differentially affect the survival and reproduction of lower-level ‘parts’ (including the genes). Organisms do not adapt to their environments in a random way as a rule (although specific behaviours, such as evasive manoeuvres, may have a random aspect). An organism's time and energy resources are limited and must be used efficiently (i.e. economically) or else. Even trial-and-error processes are purposeful. They are shaped by evolved, pre-existing search and selection criteria, namely, the adaptive needs of the organism.

These behavioural ‘choices’ may then affect the course of natural selection. Again, most important are the functional consequences for survival and reproduction of significant changes in the relationship between an organism and its environment. It is the functional effects of these changes that matter. Thus, a change in an animal's ‘habits’, or its habitat, may have no significant effect, or it could drastically change the odds of its survival. As the anthropologist Gregory Bateson (1972) famously put it, there must be ‘a difference that makes a difference’. In the process, this new habit/habitat may alter the context for the selection of various structural modifications.

One famous example involves the remarkable tool-using behaviour of the woodpecker finch. Cactospiza pallidus is one of the numerous species of highly unusual finches, first discovered by Darwin, that have evolved in the Galápagos Islands, probably from a single immigrant species of mainland ancestors. Although C. pallidus was not actually observed by Darwin, subsequent researchers have found that the woodpecker finch occupies a niche that is normally occupied on the mainland by conventional woodpeckers.

However, as any beginning biology student knows, C. pallidus has achieved its unique adaptation in a highly unusual way. Instead of excavating trees with its beak and tongue alone, as the mainland woodpecker does, C. pallidus skilfully uses cactus spines or small twigs held lengthwise in its beak to probe beneath the bark. When it succeeds in dislodging an insect larva, it will quickly drop its digging tool, or else deftly tuck it between its claws long enough to devour the prey. Members of this species have also been observed carefully selecting ‘tools’ of the right size, shape, and strength, and carrying them from tree to tree (Lack, 1961/1947; Weiner, 1994).

For our purpose, what is most significant about this distinctive behaviour is its ‘downward’ effect on natural selection and the genome of C. pallidus. The mainland woodpecker's feeding strategy is in part dependent on the fact that its ancestors evolved an extremely long, probing tongue. However, C. pallidus has no such ‘structural’ modification. In other words, the invention of a digging tool enabled the woodpecker finch to circumvent the ‘selection pressure’ for an otherwise necessary structural change. This behavioural ‘workaround’ in effect provided both a facilitator and a selective shield, or mask.

The Cybernetic Model

The science of cybernetics, which traces its origins to Norbert Weiner's (1948) foundational book Cybernetics: or Control and Communication in the Animal and the Machine, has established conclusively that goal-directed dynamic systems can no longer be considered ‘unscientific’, or be dismissed as a scientific ‘black box’. Cybernetics provides a general model for understanding biological purposiveness, or teleonomy (see especially the discussion in Mayr, 1974).

A fundamental characteristic of a cybernetic system is that it is controlled by the relationship between endogenous, in-built goals (Mayr characterized it as an internal, informational ‘program’) and the external environment. Consider this example: when a rat is taught to obtain a food reward by pressing a lever in response to a light signal, the animal learns the instrumental lever-pressing behaviour and learns to vary its behaviour patterns in accordance with where it is in the cage when the light signal occurs, so that, whatever the animal's starting position, the outcome is always the same.

The systems theorist William T. Powers (1973), in an important book and also in a paper published in Science the same year, showed that the behaviour of a cybernetic control system can be described mathematically in terms of its tendency to oppose an environmental disturbance of an internally controlled quantity.9 That is to say, the system will operate in such a way that some function of its output quantities will be almost equal and opposite to some function of a disturbance in some or all of those environmental variables that affect the controlled quantity, with the result that the controlled quantity will remain almost at its zero point. A familiar example is a household thermostat. It operates to maintain a pre-set temperature.

Needless to say, the basic thermostat model portrays only the most rudimentary example: a homeostatic system. More complex cybernetic control systems are obviously not limited to maintaining any sort of simple and eternally fixed steady state. In a complex system, overarching goals may be maintained (or attained) by means of an array of hierarchically organized sub-goals that may be pursued contemporaneously, cyclically, or seriatim. Furthermore, homeostasis shares the cybernetic stage with ‘homeorhesis’ (i.e. developmental control processes) and even ‘teleogenesis’ (i.e. goal-creating processes).

It is also important to note that cybernetic control processes are not limited only to one level of biological organization. Over the past two decades, we have come to appreciate the fact that they exist at many levels in living systems. They can be observed in, amongst other things, morphogenesis (Shapiro, 1991, 1992, 2012; Thaler, 1994), cellular activity (Hess & Mikhailov, 1994; Shapiro, 2012), and neuronal network operation (Crick, 1994), as well as in the orchestration of animal behaviour. Indeed, the cybernetic model also encompasses processes that conform to the paradigm of ‘distributed control’ or ‘horizontal control’. Some examples include bacterial colonies (Shapiro, 1988), Cnidaria (Mackie, 1990; Packard, 2006), honeybees (Seeley, 1989, 1995), army ants (Franks, 1989; Hölldobler & Wilson, 1990), slime moulds (Bonner, 1959), and, of course, humans. Indeed, Powers and various colleagues have devoted many years to developing what he calls ‘Perceptual Control Theory’, which melds cybernetics and human psychology.10 Another way to put it is that many levels of goal-oriented feedback processes exist in nature, and complex organisms such as mammals (especially socially-organized species such as humankind) are distinctive in their reliance on more inclusive, emergent, ‘higher-level’ controls.

With the increasing scope of cybernetic self-control over the course of time, a subtle but important threshold was crossed in evolution. Self-organization was augmented by the emergence of self-determination: the behavioural ability to set and pursue internally-defined behavioural goals that increasingly determine the outcome for an organism in terms of survival and reproduction.

This has had two consequences. One is that self-determining processes have gained increasing ascendancy over the ‘blind’ processes of organismic variation and natural selection. The second is that, as noted earlier, the partially self-determining organisms that are the products of evolution have come to play an increasingly important causal role in evolution; they have become co-designers of the evolutionary process, a trend that has culminated in humankind. In an extended discussion of human evolution in my book, Nature's Magic: Synergy in Evolution and the Fate of Humankind (Corning, 2003), the human species was characterized as ‘The Sorcerer's Apprentice’.

‘Teleonomic Selection’

It is clear that the traditional ways of portraying evolution, such as Monod's ‘chance and necessity’, Campbell's ‘blind variation and selective retention’, Mayr's ‘two-step, tandem process’, and Dennett's ‘blind algorithmic process’ (whatever that means), are inadequate and require modification. Evolution, similar to a wagon pulled by a team of horses, has harnessed four distinct classes of influences: chance, necessity, teleonomy, and selection. (Actually, there are five classes, counting synergy; Corning, 1983, 2003, 2005, 2007a, 2012.)

‘Chance’, meaning unpredictable ‘historical’ contingencies, is a factor at every level of life, from mutations to tsunamis. ‘Necessity’, too, is found at all levels, from the underlying laws of physics and chemistry to the ‘frozen accidents’ of the genetic code, as well as the emergent properties of the physical and biotic environment.11 (In truth, chance and necessity often cohabit, although this too is another story.) And the same is true of teleonomy and selection; all four classes of influences exist at every level in living organisms.

Another way of framing it is that evolution very often involves four distinct categories of variation: (1) molecular-genetic variation; (2) phenotypic variation (inclusive of developmental influences and behavioural variations); (3) ecological (environmental) variation; and (4) differential survival (natural selection) as an outcome of the specific organism–environment relationships and interactions in a given context. Furthermore, the causal arrows between each of these domains go in both directions.

In The Synergism Hypothesis (Corning, 1983), the role of behavioural influences in evolution was characterized as ‘Teleonomic Selection’ to highlight their purposive nature. Teleonomic Selection can be defined as: goal-related behavioural ‘choices’ among varying alternatives that may (or may not) have consequences for differential survival and reproduction, and the course of evolution over time. It refers to internally-determined (cybernetic) behavioural innovations or changes that alter the relationship between an organism and its environment.

In retrospect, it might have been more appropriate to call it ‘Neo-Lamarckian Selection’, as opposed to Darwinian Natural Selection. The proposition here is that Neo-Lamarckian/Teleonomic Selection and Natural Selection often work hand-in-hand to bring about evolutionary change. (Contrary to the current fashion, I prefer not to use Baldwin's term Organic Selection as the label for this important phenomenon. It is a clumsy term; its meaning is in dispute; it gives Baldwin undue credit; and it perpetuates the disservice to Lamarck's contribution, which Darwin himself recognized.)12

The Teleonomic Selection paradigm can be illustrated with an experiment involving the so-called crossbills, or crossbeaks, birds whose mandibles (the two parts of the beak) appear to be misaligned because they cross over at the tips. There are approximately 25 species and subspecies of these birds worldwide, including three in the Galápagos Islands, and it has been known ever since ornithologist David Lack (1961/1947) published his landmark study, Darwin's Finches, that the cross-over trait is actually adaptive. In the Galápagos, it allows the crossbills to pry open the tough seed cones of larch, spruce, and pine trees.

The question of how this peculiar trait evolved was examined in a laboratory experiment in crossbills conducted by Craig Benkman and Anna Lindholm, as described in Jonathan Weiner's (1994) The Beak of the Finch. Benkman and Lindholm first trimmed the beaks of a group of experimental crossbills (a procedure, similar to cutting your nails, that does not harm the birds). This treatment effectively incapacitated the birds; it confirmed that the cross-over alignment of the mandibles is absolutely essential for prying open the seed cones. In other words, the crossbills’ distinctive feeding strategy could not have arisen in the first place without a prior structural variation. However, the experiment also showed that, as the birds’ bills grew back, even a small degree of crossing-over was sufficient to allow them to open some of the cones, however inefficiently, and that their performance progressively improved as the beak tips regenerated.

What this experiment indicates is that, just as Darwin suggested, a ‘slight modification’ (step one) may have opened the door to a new ‘habit’ via Teleonomic Selection (step two), which natural selection subsequently ‘rewarded’ with differential reproductive success (step three). The new habit in turn established a new organism–environment relationship in which the causal arrows then flowed the other way (step four) as subsequent beak variations were ‘tested’ in relation to the new feeding strategy. The new behaviour favoured a more pronounced (more efficient) crossing-over morphology.

One other example of Teleonomic Selection involves the often indirect causal influence of behavioural choices in evolution. In the rainforest of the Olympic National Park in Washington State, there is intense competition among the towering evergreen trees (western hemlock, Sitka spruce, Douglas fir, and western cedar) inside a crowded forest canopy. Hemlocks produce by far the most seeds and are the best adapted to growing in the park (as a consequence of both competition and the weather, especially the low sunlight conditions). However, it is the Sitka spruce that dominates, and the reason is that the abundant Roosevelt elk in the park feed heavily on young hemlock trees and do not feed on the Sitka spruce. In other words, the food preference of the elk is the proximate cause of differential survival between the hemlock and spruce trees (Warren, 2010).

It should be emphasized that the basic idea underlying Teleonomic Selection is not new. As noted earlier, at the turn of the century, there was ‘Intelligent Selection’ (Lloyd Morgan) and ‘Organic Selection’ (Baldwin); in the 1920s, there was ‘Holistic Selection’ (Jan Smuts); in the 1960s, there was ‘Internal Selection’ (Lancelot Law Whyte and Arthur Koestler); and, more recently, there has been ‘Psychological Selection’ (Mundinger), ‘Rational Pre-selection’ (Boehm), ‘Purposive Selection’ (Boehm again), ‘Baldwinian Selection’ (Deacon), ‘neo-Lamarckian evolution’ (Jablonka and Lamb), and ‘Behavioural Selection’ (various authors). The Behaviorist psychologist B. F. Skinner (1981) also promoted the idea of ‘selection by consequences’ (operant conditioning). Yet another variant, ‘Social Selection’, has been deployed recently with regard to social interactions, especially in human evolution.13

Although there are some differences among these concepts, the core idea is essentially the same. Teleonomic Selection is a purposeful (cybernetic) process (i.e. an act of choosing) that always occurs in the ‘minds’ of living organisms; it is living beings that do the selecting, and it is a process that is intimately related to meeting the basic survival and reproductive needs of a given organism in a given context.14 The term Teleonomic Selection honours the fact that minds have emergent properties that allow purposeful problem-solving, innovation, and decision-making. As Patrick Bateson (2004) put it: ‘Whole organisms survive and reproduce differentially, and the winners drag their genotypes with them. This is the engine of Darwinian evolution and the reason why it is so important to understand how whole organisms behave and develop’. Bateson characterizes the role of behaviour as an ‘adaptability driver’ in evolution.15

Many years ago, Ernst Mayr drew a useful distinction between ‘proximate’ causes and ‘ultimate’ causes in evolution, concepts that are somewhat analogous to Aristotle's distinction between ‘efficient’ causes and ‘final’ causes. Proximate causes refer to the machinery of development, and to the physiology, biochemistry, and behaviour of the mature phenotype. Ultimate causes refer to the influence of natural selection, or differential survival and reproduction (Mayr, 1976: 695–696).16

In practice, proximate and ultimate forms of causation interpenetrate; proximate causes associated with what I call Teleonomic Selection may also be responsible for shaping ultimate causes. Behavioural choices may be the effective cause of natural selection. As noted earlier, Teleonomic Selection is implicated in habitat choices, adaptive radiations, dietary choices, predator–prey interactions, and even what Lynn Margulis (after Mereschkovsky) calls ‘symbiogenesis’ (Margulis, 1970, 1981; also Margulis & Fester, 1991). Indeed, the proximate causes of novel forms of symbiosis, from lichens to such evolutionary turning points as the origin of eukaryotic cells, as well as the emergence of land plants and animals, the evolution of birds, and even the development of social organization, were most likely the result of various behavioural ‘initiatives’. In short, many of the ‘tipping points’ in evolution (in Malcolm Gladwell's term; Gladwell, 2000), or what Niles Eldredge & Stephen Jay Gould (1972) characterized as a ‘punctuated equilibrium’, can be attributed to behavioural innovations and Teleonomic Selection as a major causal agency.

Similarly, the many kinds of ‘artificial selection’ practiced by farmers and plant breeders, inclusive of the more sophisticated technologies associated with genetic engineering, can also be redefined as examples of Teleonomic Selection: purposeful behavioural selections by third-parties that shape the course of natural selection in other species. ‘Sexual selection’ is also an example of Teleonomic Selection. Mate-choices among reproductive animal pairs involve behavioural choices that may directly shape the course of evolution, as Darwin himself first pointed out.

Teleonomy and Our Evolutionary Future

As the history of H. sapiens clearly illustrates, teleonomy and self-determination have increasingly influenced the overall course of the evolutionary process. Cybernetics, information science, and semiotics (i.e. the science of signs and meanings) have illuminated and highlighted the emergent and ever-expanding role of intelligence in evolution.17 Indeed, it is important to remember that automobiles, airplanes, moon rockets, the Internet, and iPads are also products of the evolutionary process (i.e. of evolved intelligence).

However, this does not lend support to the other aspect of Lamarck's thinking: his vision of an overarching direction or goal in evolution. Dobzhansky appropriately characterized evolution as a ‘grand experiment in adaptedness’: an open-ended challenge, and an adventure, with an ultimate outcome that cannot be foretold.

As is the case with other living organisms, humankind tends to focus on solving the immediate problems of living in a given economic and cultural context; our evolutionary trajectory has entailed, in essence, an economic process (in a broad sense) involving means and ends, and costs and benefits, in relation to the ongoing challenge of survival and reproduction. It has not been our purpose (as a general rule) to follow some grand evolutionary path or societal goal, and any pretensions in this regard have generally fallen short; previous generations of evolutionists were doomed to be disappointed in their visions of evolutionary ‘progress’. Indeed, natural selection slavishly adheres to the law of unintended effects. We would be better advised to focus on the currently popular buzzword: ‘sustainability’. This will be quite enough of a challenge for the foreseeable future.


  1. 1

    Although Lamarck was often accused, even by Darwin, of proposing that new habits arise as a result of spontaneous ‘volition’ or ‘desire’, he said no such thing. This misapprehension was the apparent result of a mistranslation of the French word besoin; the word volonté was used by Lamarck only in relation to some ‘higher’ animals. Indeed, Lamarck viewed behavioural changes, by and large, as a matter of challenge and response, of externally stimulated creativity rather than a spontaneous impulse, a formulation that is quite compatible with the modern concept of phenotypic plasticity; see also Cannon (1955, 1959) and Gissis & Jablonka (2011).

  2. 2

    Baldwin made ambitious claims for the role of Organic Selection. However, his early writings were anticipated by Lloyd Morgan's (1896a) in-depth treatment in his book, Habit and Instinct, and his lecture that year at the New York Academy of Science. Following Lloyd Morgan, Baldwin spoke of behavioural ‘accommodations’ that could keep an animal alive and so allow its offspring to ‘accumulate’ biological ‘variations’ determining evolution in ‘subsequent generations’. Indeed, Baldwin, in his 1902 book, stressed the possibility of varying relationships between learned accommodations and ‘coincident [congenital] variations’, as did Lloyd Morgan (Baldwin, 1902: 149).However, Simpson (1953) chose to define the Lloyd Morgan/Baldwin effect much more narrowly as pertaining only to parallel ‘genetic changes with similar results’. Thus, to use one of Simpson's examples, if a callous acquired by a human hand through use made an appearance in the hand of a newborn and was favorably selected, this would be an instance of the Baldwin effect. (How this differs from C. H. Waddington's concept of genetic assimilation is unclear.) No wonder Simpson concluded that the Baldwin effect was unproven and, in any case, of no great importance. However, subsequent Baldwin champions bypassed Simpson's definition in favour of more expansive interpretations (West-Eberhard, 2003: 25–25; 151–153), just as future generations of evolutionists (Simpson among them) came to see behaviour as a major change agent in evolution without reference to Baldwin or Lloyd Morgan, much less Lamarck.

  3. 3

    A sampler of more recent contributions includes Thorpe (1978), P. Bateson (1988, 2004, 2005), P. Bateson & Gluckman (2011); P. Bateson, Klopfer & Thompson (1993), Plotkin (1988), Wcislo (1989), West-Eberhard (1989, 2003, 2005), Wills (1993), Boehm (1991), Byrne (1995), Margulis & Sagan (1995), Jablonka & Lamb (1995), Avital & Jablonka (2000), Jablonka, Lamb & Avital (1998), Heyes & Huber (2000), Kull (2000), Yoerg (2001), Wynne (2001), Grether (2005), Pigliucci, Murran & Schlichting (2006), Crispo (2007, 2008), Auletta (2010), and Moczek et al. (2011).

  4. 4

    The research on animal decision-making goes back more than 40 years to the seminal work on optimal foraging theory by MacArthur & Pianka (1966), Emlen (1966), Schoener (1971), Charnov (1976), amongst others. There is also the large and rapidly growing research literature in the field of ‘behavioural ecology’, which utilizes explicit economic analyses of animal behaviour. See especially the benchmark volumes edited by Krebs & Davies (1984, 1991, 1993, 1997); see also the volume on Cognitive Ecology edited by Dukas (1998); and the volume on Economics in Nature edited by Noë, Van Hooff & Hammerstein (2001). Also notable was the early use of explicitly economic concepts and analyses by Marion Stamp Dawkins (1983, 1988) and the empirical work of Christopher Boehm (1991).

  5. 5

    Shapiro argues that even cells must be viewed as complex, teleonomic systems that control their own growth and reproduction, and shape their own evolution over time. He refers to it as a ‘systems engineering’ perspective. Indeed, there is no discrete DNA unit that fits the neo-Darwinian model of a one-way, deterministic ‘gene’. Instead, the DNA in a cell represents a two-way, read-write system wherein various ‘coding sequences’ are mobilized, aggregated, manipulated, and even modified by other genomic control and regulatory molecules in ways that can also influence the course of evolution itself. Some of the many examples Shapiro cites include immune system responses, chromosomal rearrangements, diversity generating retro-elements, the actions of DNA transposons, genome restructuring, whole genome duplication, and symbiotic DNA integration.

  6. 6

    This issue involves some basic misunderstandings relating to cybernetics (the science of communications and control processes in goal-oriented systems) and its relationship with other kinds of dynamic processes associated with complexity theory. The issue is dealt with in some depth in Corning & Kline (1998a, b) (see also Corning, 2005, 2007b) under the heading of ‘control information theory’. Two important book-length treatments of this issue are Cziko's Without Miracles (Cziko, 1995) and The Things We Do (Cziko, 2000).

  7. 7

    Although Monod did utilize the term ‘teleonomy’ to characterize living organisms, he called it a ‘profoundly ambiguous concept’ (Monod, 1971: 14). He also used the term in a very constricted, mechanistic way as a synonym for the ‘quantity of information’ that is ‘transmitted’ in reproduction and ontogeny. To his credit, he also recognized that living systems are cybernetic systems (see below). However, he did not view teleonomy explicitly as an independent causal agency in evolution.

  8. 8

    See the ‘target article’ by Dennett (1983) and accompanying commentaries. The concept of ‘mind’ as a factor in evolution dates back to the extensive work in comparative psychology during the latter part of the 19th Century, much of which was rejected and all but forgotten in the 20th Century. See especially Romanes (1883), Lloyd Morgan (1891, 1896a, 1908/1900, 1923), Thorndike (1965/1911), and Hobhouse (1915). More recent discussions relating to the ‘mind’ and nature of animal intelligence can be found in Griffin (1992, 2001), Gould & Gould (1994), Cziko (1995, 2000), Bekoff & Jamieson (1996), Rogers (1998), and Corballis & Lea (1999).

  9. 9

    There is a very large research literature and several journals devoted to cybernetics and control systems, with robotics being a cutting-edge area at the present time. For a review that includes a new approach to information theory called ‘control information’, see Corning (2007b); see also Cziko (1995, 2000) and Powers’ Perceptual Control Theory (see endnote 10).

  10. 10

    Over the past 40 years, Powers has greatly elaborated on Weiner's seminal ideas and has applied the control system model specifically to human behaviour in ways that can readily be tested. Powers observes that ‘Perceptual Control Theory may have a long way to go as a theory of human nature, but it's the only theory that deals with individuals and accepts them as autonomous, thinking, aware entities’ (Powers, 2010/1989: 5). He points out that learning is not about ‘stimuli’, as psychologists have long hypothesized but, instead, it is about perceptions and how they are interpreted. It is perception that controls behaviour. ‘A control system senses some aspect of its environment and produces actions bearing directly on that aspect’ (Powers, 1995). Among the other relevant publications, see especially Powers (1989, 1992, 1998, 2008, 2010/1994) and Forsell (2010).

  11. 11

    The term ‘frozen accidents’ is unfortunate. Many of these primordial evolutionary ‘inventions’ have been ‘procreative’, important enablers for further evolutionary developments. Moreover, their preservation over the course of evolutionary history has been anything but accidental. They represent solutions to functional problems that are ‘conserved’ because they work; they serve the functional needs of living systems. For example, there is research suggesting that it is possible to have more than four DNA bases. However, four are sufficient, just as four wheels are sufficient for the functional needs of automobiles. In other cases, functional solutions are far from being ‘frozen’ in place. Photoreceptors (eyes), for example, have been reinvented many times (one estimate puts it at more than 40). Also, they operate on a variety of different functional principles, from pinholes to multiple tubes, movable lenses, and fixed focusing lenses similar to our own.

  12. 12

    An example of this muddle can be found in the volume edited by Weber & Depew (2003), which provided a reconsideration of the Baldwin effect by several scholars. (See also the critical book review by Bateson, 2004.) Bateson noted that the book fell short in clarifying the role of behaviour in evolution: ‘The focus is too narrow because the book has not captured the major conceptual changes that have been taking place in biology in the last fifteen years’.It should also be noted that the idea of behavioural changes as an influence in evolution was hardly a new idea in 1896. In addition to Lamarck and Darwin (and D. A. Spalding, 1873, as Patrick Bateson, 2004, has pointed out), August Weismann, the founding father of modern genetics and a contemporary of Baldwin, was also familiar with the idea of phenotypic plasticity. More importantly, the British comparative psychologist and animal behaviour specialist Conwy Lloyd Morgan (1891, 1896a, 1908/1900) discussed the idea in his many writings, including three books on animal behaviour: Animal Life and Intelligence, Habit and Instinct, and Animal Behaviour.Indeed, the Baldwin effect should perhaps be called the Lloyd Morgan effect. Lloyd Morgan's (1896a) book Habit and Instinct represents an in-depth analysis of the relationship between learned (‘acquired’) and ‘congenital’ influences in behaviour, with entire chapters devoted to how habits are developed, the role of imitation and emotions, how intelligence evolves, and three chapters on what later became known as Organic Selection (all of which was supported with many examples). Lloyd Morgan spoke of developments that are ‘the result of conscious choice and selection’, which is ‘dependent upon an innate power of association’ and ‘individual experience to give it actuality and definition’ (p. 157). Subsequently, he discussed at length the role of ‘intelligence’ and characterized mental evolution as ‘a new method of evolutionary progress’ (p. 271). And in his chapter on ‘Modification and Variation’, Lloyd Morgan detailed the thesis underlying the Organic Selection idea in twenty numbered propositions. Among other things, he wrote that ‘persistent [learned] modifications through many generations, though not transmitted to the germ, nevertheless affords the opportunity for germinal variation of like nature’ (p. 319). He noted further that, when a group of ‘plastic’ organisms is placed under new conditions, those that are ‘equal to the occasion are modified and survive … There is no transmission of the effects to the germinal substance’ (p. 320). However ‘any congenital variations similar in direction to these modifications will tend to support them … Thus will arise congenital predispositions to the modifications in question … plastic modification leads, and germinal variation follows. The one paves the way for the other’ (p. 320). Lloyd Morgan concluded that ‘plastic modification and germinal variations have been working together all along the line of organic evolution to reach the common goal of adaptation’ (p. 321).It is true that Baldwin, an American child psychologist by training (see Baldwin, 1895), coined the term ‘Organic Selection’. However, it is also clear that he did not coin the idea and, at first, he incorrectly promoted it as a ‘new factor’ in evolution, claiming that it was neither Lamarckian, nor Darwinian. Apparently, he was disabused of this claim at the lecture given by Lloyd Morgan at the New York Academy of Science early in 1896, which Baldwin attended.Thereafter, there was a flurry of short publications on the subject by Baldwin, Lloyd Morgan, and palaeontologist Henry Fairfield Osborn in the pages of the then new journal Science. Baldwin also published an article about it in the American Naturalist and discussed it further in a book (Baldwin, 1902). Finally, contrary to the many later misinterpretations of the term, Baldwin (1896c) himself defined Organic Selection strictly with reference to ‘acquired’ behavioural ‘choices’, regardless of their consequences. The term had no inherent evolutionary significance. It only provided a label for Lamarck's (1984/1809) ‘changes of habits’, for Spalding's (1873) ‘Robinson Crusoe’ effect, and for Lloyd Morgan's (1896a, b) ‘intelligent selection’.

  13. 13

    Social selection refers, for the most part, to social/cultural decision-making processes (Teleonomic Selection at the social group level) that affect the gene pool of a group, although some define it more broadly in terms of social interactions of any kind. Social selection has been invoked especially with regard to the evolution of social cooperation and altruism in humankind, with social rewards and punishments being viewed as playing an important role. It is an influence that Charles Darwin also recognized in The Descent of Man (Darwin, 1874/1871). One concern is that some theorists treat the consequences for differential survival and reproduction as being distinct from natural selection (Wolf, Brodie & Moore, 1999). For more on this important concept, see Stark (1961), Simon (1990), Tanaka (1996), West-Eberhard (2003), Frank (2005), Hodgson & Knudsen (2006), and Boehm (2008).

  14. 14

    A particularly significant class of examples includes the many different forms of collective violence in nature, behaviours that require a close assessment of risks, costs, and benefits (Corning, 2007a). For more detailed discussions of Teleonomic Selection and various alternative formulations, see Corning (1983, 2003). It should be stressed that Teleonomic Selection does not encompass all of the varied phenomena that are included in the term ‘phenotypic plasticity’. Thus, differential survival as a result of the ability of different individual genotypes to tolerate extreme environmental conditions (e.g. heat or cold stress) would not be examples of Teleonomic Selection. That would be natural selection, pure and simple. Nor would environmental influences that alter a ‘plastic’ morphology during the development. However, building a fire to keep warm would entail Teleonomic Selection. Conversely, under West-Eberhard's definition, animal problem solving and innovative behaviours would not strictly speaking qualify as examples of phenotypic plasticity. Indeed, words such as ‘teleonomy’, ‘purposiveness’, and ‘problem solving’ are not found in West-Eberhard's extensive index, although the term ‘key innovation’ is mentioned under the subject of adaptive radiations, along with many references to ‘learning’.

  15. 15

    Bateson identifies four distinct ways in which behaviour can affect evolution: (1) when animals make active choices among alternatives; (2) when their behaviour changes their physical and social environment (the context of selection); (3) when animals respond to changing conditions; and (4) when animals take the initiative and expose themselves to novel conditions; see also Bateson (2005, 2010), Bateson & Gluckman (2011), and Wcislo (1989).

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    An especially useful discussion of the relationship between proximate and ultimate causation can be found in Stamps (1991); see also Jablonka et al. (1998). Patrick Bateson (pers. comm.) points out that the pioneer ethologist Nikolaas Tinbergen developed a four-fold distinction between control, development, function, and evolution that also provides a useful heuristic framework for studying animal behaviour (Tinbergen, 1965). However, Mayr's two-way distinction, which focuses on the outcomes that result from any given behaviour, is more widely known and understood.

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    See especially Corning (2007b), Hoffmeyer (1997), and Hoffmeyer & Kull (2003). One concern about semiotics is that it appears to be insulated from the science of cybernetics. The concept of primordial ‘signs’ may also be insufficient to encompass the broader biological concept of ‘perception’ (i.e. the ability of organisms to sense and extract ‘meanings’ from various aspects of their environments, e.g. gravity, sunlight or air temperatures). Indeed, even the absence of something (e.g. water, oxygen or sunlight) may be sensed and used by living organisms.