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Biological Journal of the Linnean Society, 2014, 112, 242–260.
Evolution ‘on purpose’: how behaviour has shaped the
evolutionary process
PETER A. CORNING*
Institute for the Study of Complex Systems, 620 NE Vineyard Lane, #B-303, Bainbridge Island, WA
98110, USA
Received 6 December 2012; revised 10 January 2013; accepted for publication 10 January 2013
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.
ADDITIONAL KEYWORDS: Baldwin effect – cybernetics – genetic assimilation – natural genetic engineering – Organic Selection – phenotypic plasticity – synergy – teleonomy.
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-andsuccess’ process and a deterministic directional
process, whether divinely sanctioned or as the result
*E-mail: [email protected]
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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
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 242–260
BEHAVIOUR AND THE EVOLUTIONARY PROCESS
highlighted especially in work on ‘phenotypic plasticity’ (West-Eberhard, 1989, 2003, 2005; Pigliucci,
2001), ‘niche construction theory’ (Laland, OdlingSmee & 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, energycentred ‘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
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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.
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 242–260
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P. A. CORNING
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 genecentred view of evolution. As he pointed out, ‘It is the
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BEHAVIOUR AND THE EVOLUTIONARY PROCESS
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
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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, trialand-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’.
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P. A. CORNING
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 sloweracting 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
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BEHAVIOUR AND THE EVOLUTIONARY PROCESS
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
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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 partialautonomy 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
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P. A. CORNING
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
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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 valuedriven 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 purpose-
249
ful 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 toolusing 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,
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P. A. CORNING
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 goaldirected 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 internallydefined behavioural goals that increasingly determine
the outcome for an organism in terms of survival and
reproduction.
This has had two consequences. One is that selfdetermining 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,
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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 internallydetermined (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,
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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 crossingover 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
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P. A. CORNING
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 everexpanding 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
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BEHAVIOUR AND THE EVOLUTIONARY PROCESS
‘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.
4
ENDNOTES
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 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 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),
5
6
7
8
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Grether (2005), Pigliucci, Murran & Schlichting (2006),
Crispo (2007, 2008), Auletta (2010), and Moczek et al.
(2011).
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).
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 retroelements, the actions of DNA transposons, genome
restructuring, whole genome duplication, and symbiotic
DNA integration.
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).
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.
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
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 242–260
254
9
10
11
12
P. A. CORNING
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).
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).
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).
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.
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)
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 242–260
BEHAVIOUR AND THE EVOLUTIONARY PROCESS
13
14
15
16
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’.
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).
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’.
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).
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
255
(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.
17 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.
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