Abstract

Charles Darwin’s concept of “Natural Selection” was an important step forward, theoretically. It recognized the key fact that life on Earth is a contingent, always at-risk process, and that living systems are embedded in a natural environment that is filled with variable opportunities and threats. On the other hand, Darwin failed to acknowledge the fact that all living systems – from the smallest single-celled bacteria to humankind – are also shaped by their evolved purposiveness (teleonomy). Their initiatives and activities – their behavior – has exercised an important influence over the trajectory of life on Earth, as one of Darwin’s predecessors, Jean-Baptiste de Lamarck, fully appreciated. Today we know that there have been many shaping influences in evolution. Most important, perhaps, is the fact that life has also been a multi-faceted cooperative (synergistic) enterprise over time. However, the proposed Inclusive Synthesis is also open-ended, because it is expected that more has yet to be learned about the history of life on Earth. 

Keywords

Evolution, Teleonomy, Behaviour, Cooperation, Synergy.

Highlights

• Darwin discounted the role of purposive behaviour in evolution
• The “Modern Synthesis” attributed evolution to “random” genetic mutations 
• The purposiveness (teleonomy) of living systems has also shaped evolution
• We now know of many other influences in evolution as well
• Various cooperative effects (synergies) have also been important

Introduction

Charles Darwin’s theory of biological evolution, featuring his novel concept of “Natural Selection”,¹ represented an important step forward in our enduring efforts to understand/explain the rise and development of living systems over time. Darwin’s theory was based on the fundamental fact that life on Earth is a contingent, always at-risk process that is embedded in a variable, often challenging environment, including many opportunities and threats. (Darwin called it “the struggle for existence”.)

During the twentieth century, in the era in evolutionary theory widely known for what was called “The Modern Synthesis” (inspired by the title of biologist Julian Huxley’s landmark 1942 book, “Evolution: The Modern Synthesis”) random genetic mutations came to be viewed as the primary source of innovation and change in living systems.² (This was not actually Huxley’s own view. It was inspired by the pioneering work in genetics, and the theoretical claims, of the biologist Auguste Weismann [1892],³ and was reinforced by such things as the work of biologist W.D. Hamilton⁴ and the influential popular book, “The Selfish Gene”, by biologist Richard Dawkins.⁵  

Over the course of the past century, however, we have come to realize that there are a great many things that have influenced the trajectory of life on Earth. (I will summarize some of these below.) Perhaps most important was the recognition that living systems have been active participants in the evolutionary process – a major shaping influence and a co-determinant of the history of life. This was fully appreciated by a well-known but often discounted/mistreated predecessor of Darwin, the 18^th century naturalist/biologist Jean-Baptiste de Lamarck. Darwin himself discounted it. (I will also review this episode below,) 

Another important aspect of our revised/refined view of evolution is the recognition that it has not been a predominantly competitive process – as portrayed by Darwin himself and memorably characterized by the poet, Alfred Lord Tennyson, as “nature, red in tooth and claw” – but it was, in many different ways, a cooperative (synergistic) process.^6-9 These and other developments in evolutionary biology are incorporated here into what I am calling a more “inclusive” theoretical synthesis. 

 

The Evolution of Living Systems

In his two important books on the subject, biochemist Nick Lane,^10,11 discussed at length the evidence for how life arose. As he put it: “Life itself transformed our planet from the battered and fiery rock that once orbited a young star…Life itself turned our planet blue and green, as tiny photosynthetic bacteria cleansed the oceans of air and sea and filled them with oxygen. Powered by this new source of energy, life erupted”.¹⁰ 

How life first arose has long been debated, of course. In the modern era, the debate began, perhaps, with the Nobel physicist Erwin Schrödinger’s wartime lectures and famous 1944 book, What is Life? Schrödinger pioneered the idea that ordered energy (now called negative entropy, or “negentropy”) was an essential factor.¹² Life is, among other things, a thermodynamic process. Today, we commonly refer to it as “metabolism”. Many years later, biologists Humberto Maturana and Francisco Varela (1980/1973) identified another important property of living systems.¹³ They called it “autopoiesis” or self-making. Life has a form of autonomy, they proposed. Today the term “agency” is commonplace.[1] 

A more elaborate effort to explain the rise of living systems was provided by the little-known Hungarian theoretical biologist Tibor Gánti.¹⁴ His three-part “Chemoton” model included an autocatalytic network for metabolism, machinery for controlling growth and self-replication, and a protective envelope to shield the system from the environment. In other words, he proposed a cooperative (synergistic) system. Some theorists, notably including John Maynard Smith and Eórs Szathmáry (1999),¹⁵ argue that an additional requirement for life is the ability to evolve, when there is variation that can be differentially selected. I would add that life must also be able to respond to “feedback” and to changes in the environment. It must be sentient.  

Two of the major alternative theories about the origin of life depend on yet another synergistic effect, an external catalyst. One is the “surface metabolism” theory of Günter Wӓchtershӓuser (1988).¹⁶ He proposed that ancient Earth, with high concentrations of metallic compounds, may have provided important catalysts. The subsequent discovery of hydrothermal vents on the ocean floor lent credence to this idea. The other theory, proposed by geochemist Mike Russell (2006)¹⁷ and his colleagues,^18,19 involve a different kind of “metabolism first” theory, namely deep-sea alkaline vents and the CO₂ in the ancient oceans. In effect, this provided an abundant source of free energy. It is a compelling idea. Most recently, biochemists Robert Pascal and Addy Pross have suggested that consciousness/cognition in evolution may have a biochemical basis.^20,21 

These and other theories advanced in recent years, like the proposal that life was “seeded” by compounds brought from outer space by the once abundant meteors,²² make it seem even more likely that a synergistic combination of elements for the catalyzing life arose together in the early environment. 

The evolution of prokaryotes (bacteria and their cousins, archaea) perhaps 3.7 billion years ago (some theorists say even earlier) was another major step in biological evolution. The prokaryotes were the first complete organisms, and they are still with us today. Indeed, they are the most productive form of life on Earth, with an estimated total biomass that outweighs all other fauna and flora combined.⁹ Prokaryotes are also highly creative and adaptable. They invented many important biotechnologies, including photosynthesis, nitrogen fixing, fermentation, and cellular damage repair, and they can synthesize many different kinds of minerals. More important for our purpose, they invented various forms of collective action, from the division of labor to pack-hunting behaviors. It was the primordial “collective survival enterprise”.⁹ As Baluśka, Miller & Reber (2023a,b)^23,24 have stressed in detail, sentience and cognitive abilities can be found in all living organisms. Some theorists even see evolution as a cognition-based process.²⁵ 

The next major transition in evolution was the emergence, some 1.8-2.0 billion years ago, of eukaryotes – complex single-celled organisms with an array of specialized internal organelles and with genes in a sequestered nucleus. But the most important innovation was the role played by their symbiotic partners, the mitochondria, which provide the eukaryotes with an abundant source of energy. This enabled them to grow vastly larger than the prokaryotes – an important synergy of scale – and to become specialists in even larger multicellular organisms, another transition in biological size and complexity. “Symbiogenesis” represented an important cooperative partnership[2].^26-39 

The emergence of multicellular organisms was another synergistic innovation. Among the innumerable examples, consider the human body. It involves an extraordinary combination of labor by an estimated 30 trillion cells of some 210 different kinds that are organized into an extraordinarily complex system of functionally differentiated parts, including 10 specialized organ systems (pp. 112-113).⁹ A human being, or any other multicellular organism (from earthworms to elephants) is fundamentally a cooperative effect, a synergistic system.  

Finally, the synergies were raised to a new level with the emergence of behavioral cooperation and social organization among individuals of the same species – including everything from pack hunting to joint nesting, collective migration, collective defence against predators, and much more. One well-known example is the so-called leaf-cutter ants (pictured on the cover of my 2018 book, Synergistic Selection: How Cooperation has Shaped Evolution and the Rise of Humankind). Another example is the recent discovery of underground cooperative systems among forest trees.⁴⁰ 

Teleonomy in Evolution

“Vitalism” is the doctrine that proceeds from the premise that living organisms are fundamentally different from non-living entities because they contain some non-physical element or are governed by different principles than inanimate things. Frequently used are such terms as "élan vital" or a “vital spark” (coined by Vitalist Henri Bergson). Among other things, this doctrine has come to be associated with the Intelligent Design movement, as well as various therapeutic medical treatments. Since the mid-twentieth century, though, Vitalism has been considered a pseudoscience. In Nobel biologist François Jacob’s (1977) classic term, evolution can be characterized as a process of biological “tinkering” (or trial-and-error) over eons of time.⁴¹    

Now it seems that Vitalism is being revitalized. Daniel Witt (2024),⁴² a persistent advocate for the idea of Intelligent Design, has suggested that recent publications on purposiveness (teleonomy) in living systems show that Vitalism is “making a comeback.” Witt does not seem to believe that teleonomy in living systems could be an evolved biological trait – a product of natural selection. This view is rebutted in the extensive introductory/overview chapter: “Teleonomy in Evolution: “The Ghost in the Machine” in PA Corning, et al., eds., (2023).⁴³ As the eminent twentieth century biologist Theodosius Dobzhansky long ago explained:     

Purposefulness, or teleology, does not exist in non-living 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.⁴⁴   

In sum, purposiveness (or teleonomy) in living systems is a product of evolution and natural selection. It has nothing to do with any purported external Vitalism.⁴⁵   

However, evolved purposiveness in biological evolution is not simply a product of natural selection. It is also an important cause of natural selection and has been a major shaping influence in evolution over time. Natural selection is not an exogenous force or “mechanism”. It is an outcome of the relationships and interactions between purposeful living organisms – “agents” – and their lived-in environments, inclusive of other organisms.  The term “teleonomy” was originally coined by the biologist Colin Pittendrigh in connection with the landmark 1957 conference on behavior in evolution.⁴⁶ Pittendrigh was seeking to draw a contrast between an “external” teleology (Aristotelian or religious) and the “internal” purposiveness and goal-directedness of living systems, which are the products of the evolutionary process, and of natural selection.     

Many theorists over the years have expressed supportive views, as Samir Okasha⁴⁷ has documented in his book-length study, Agents and Goals in Evolution (see also Walsh, 2015).⁴⁸ For instance, the Nobel biologist Jacques Monod (1971:9)⁴⁹ concluded that “one of the most fundamental characteristics common to all living things [is] that of being endowed with a project, or a purpose.” Likewise, the biologist Ernst Mayr, one of the founding fathers of the Modern Synthesis in evolutionary biology, wrote “goal directed behaviour…is extremely widespread in the natural world; most activity connected with migration, food-getting, courtship, ontogeny, and all phases of reproduction is characterized by such goal orientation”.^50,51    

Over the years, many theorists have interpreted teleonomy broadly. Pittendrigh (1958)⁵² himself characterized it as a “fundamental property” and defining feature of all biological phenomena, including behavior. Similarly, Monod, in his influential book, Chance and Necessity, concluded: “All the structures, all the performances, all the activities contributing to the essential project [of life] will hence be called ‘teleonomic’…. It is the very definition of living beings”.⁴⁹ As an example, Monod pointed to the central nervous system.     

However, Mayr (1974),⁵³ in his classic essay on “Teleological and Teleonomic: A New Analysis,” opposed such a broad definition. Mayr framed teleonomy as requiring a pre-existing goal and “something material” that guides and controls a “process” to a “determinable end.” In living organisms, he said, this a priori goal entails a “program” – an analogy Mayr borrowed from computers. It is the teleonomic program that is responsible for directing the process of developing a phenotype and its behavior, although an “open program” (as Mayr called it) allows for the influence of learning and experience (and other “disturbances”). To illustrate his definition, Mayr alluded to the science of cybernetics, or goal-directed control systems. He also insisted that a teleonomic program – an obvious euphemism for the genome – could only have a one-way flow of information, and that developmental influences are highly restricted. “The inheritance of acquired characters becomes quite unthinkable.” (In fact, we now know this is not true.)     

Mayr was adamant that it was inappropriate to attribute purposiveness to the process of evolution itself, or to the influence of natural selection, and he opposed applying the term teleonomy to any “static” biological system (presumably meaning the structural components of an organism). He cited the central nervous system as a contrary example. Thus, he implicitly contradicted Monod. Mayr also insisted that: “It is misleading and quite inadmissible to designate such broadly generalized concepts as survival or reproductive success as definite and specified goals. Teleonomy does not exist outside the ultimately determinative influence of DNA and the genetic ‘program’.”     

In other words, Mayr was supportive of the gene centered, one-way, bottom-up evolutionary paradigm, referred to as the Modern Synthesis or Neo-Darwinism, which predominated at the time in evolutionary theory, and he seemed to exclude what he called “proximate” causes from exerting a direct influence on “ultimate” causes (natural selection and evolution). Indeed, in an earlier paper, Mayr (1961) had identified only two categories of legitimate “evolutionary causes” – “genetic causes” and “ecological causes.⁵⁴”     

Mayr’s adherence to what the Nobel biologist Francis Crick (1970)⁵⁵ termed the “central dogma” of the gene-centered evolutionary theory and his radical separation of proximate and ultimate causation is, in fact, no longer tenable.^56-61

Beyond the Selfish Gene

As noted above, there is growing evidence that symbiosis – cooperative relationships between organisms of different species with complementary capabilities – is a widespread phenomenon in the natural world, and that “symbiogenesis” has played a major causal role in shaping the evolutionary trajectory over time.^26-32,62-67 Symbiogenesis theory shifts the locus of innovation away from “random” changes in genes, genomes, and the “classical” model of natural selection to the “purposeful”, cooperative behavioral actions of the phenotypes and their functional consequences.   

Another challenge to the Modern Synthesis version of evolution – what the anthropologist Sherwood Washburn called “genitis,” or “the genetic disease” -- was the discovery that single celled prokaryotes are profligate sharers of genetic material via “horizontal” (or lateral) gene transmission and do not strictly follow the pattern of competition and Mendelian (“vertical”) inheritance from parent to offspring, as the Modern Synthesis assumes.^63,68,69 The biologist Eugene Koonin (2009)⁷⁰ concluded that all the central tenets of the Modern Synthesis break down with prokaryotes and the findings of comparative genomics. The prokaryote world can best be described as a single, vast, interconnected gene pool, he argues.   

The rise of evolutionary developmental biology (evo-devo for short) has also produced serious challenges to the Modern Synthesis, including the discovery that there are many deep homologies and highly conserved structural gene complexes in the genome (some of which are universal in living systems), and especially the extensive work on morphological development and “phenotypic plasticity.”^68,71-75  

There is also the burgeoning evidence that the genome is in fact a “two-way read-write system,” as the biologist James Shapiro (2011, 2013) characterizes it.^76,77 The extensive and rapidly increasing evidence of epigenetic inheritance (changes in the phenotype that are transmitted to the germ plasm in the next generation) also falsifies the one-way, gene-centered theory.^78-85   

Recent progress in microbiology has also shown that an overwhelming majority of DNA changes in the genome are the result of internal regulatory and control networks, not random mutations and incremental, “additive” selection. In fact, rapid genome alteration and restructuring can be achieved by a variety of mobile DNA “modules” -- transposons,⁸⁶ integrons, CRISPRS, retroposons, variable antigen determinants, and more.^{63,68,76,77,83,87-89}   

It is now also apparent that individual cells have a great variety of internal regulatory and control capabilities that can significantly influence cell development and the phenotype. They may even provide feedback that modifies the genome and affects subsequent generations.^{68,76,83,84,90-93} Particularly significant are the discoveries related to the influence of exosomes, which resemble Darwin’s speculative idea of pangenesis and the role of internal migratory “gemmules” in reproduction.⁹⁴ Exosomes also clearly violate the so-called Weismann Barrier (1892),³ the assumption that genetic change can only be a one-way process. 

As Shapiro (2011:2) emphasizes,⁷⁶ “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 cites some 32 different examples of what he refers to as “natural genetic engineering,” including immune system responses, chromosomal rearrangements, diversity generating retroelements, the actions of transposons, genome restructuring, whole genome duplication, and symbiotic DNA integration.^77,95,96 

Likewise, Jablonka and Lamb (2014)⁸⁰ identify four distinct “Lamarckian” modes of inheritance: (1) directed adaptive mutations, (2) the inheritance of characters acquired during development and the lifetime of the individual, (3) behavioral inheritance through social learning, and (4) language-based information transmission. All this prompted biologist Kevin Laland and his colleagues to publish two major critiques of Mayr’s proximate-ultimate dichotomy.^56-57 These critics argue that proximate and ultimate causes are interpenetrated and that the one-way causal model associated with the Modern Synthesis and Neo-Darwinism should be replaced with one that recognizes a major role for “reciprocal causation”.^58,59

Teleonomy and Natural Selection

To fully appreciate the causal role of teleonomic influences in evolution, we believe it would be helpful to revisit the concept of natural selection. The neo-Darwinian definition of the term has always tended to be narrow, gene-centered, and circular. Evolution is defined as "a change in gene frequencies" in a given “deme”, or breeding population, and natural selection is defined as a "mechanism " which produces changes in gene frequencies. “Changes in the frequencies of alleles by natural selection are evolution,” as the biologist John H. Campbell put it in a review.⁹⁷ By implication, it followed that mutations and related molecular-level changes – subject to the “approval” of natural selection – are the only important sources of novelty in evolution. Natural selection is in turn represented as being an external “mechanism”, or “force” out there in the environment somewhere.  

The dominant theme in this paradigm is a competitive “struggle for existence,” as Darwin characterized it. (The associated catch phrase, “survival of the fittest,” was actually coined by a contemporary theorist, Herbert Spencer, but it was also used by Darwin in later editions of his masterwork). Indeed, the term “Darwinian” is often treated as a synonym for any competitive, winner-take-all dynamic. However, it happens that this is only one of Darwin’s two distinct evolutionary theories. The other theory, less appreciated, actually originated with his prominent predecessor, Lamarck (see below).   

However, natural selection is not a mechanism; it is a happening. 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 the environment. In fact, the term natural selection, as Darwin used it, is a metaphor – an “umbrella term” that identifies a fundamental aspect of the evolutionary process. The ground zero premise of evolutionary biology is that life is, in essence, a contingent “survival enterprise.” Living organisms are inherently contingent dynamic phenomena that must actively seek to survive and reproduce. This existential problem requires that they must be goal-directed in an immediate, proximate sense. Thus, natural selection refers to whatever functionally significant factors are responsible in a given context for causing differential survival and reproduction. The well-known Behaviorist psychologist B.F. Skinner (1981)⁹⁸ called it “selection by consequences.” Properly conceptualized, these causal "factors" are intensely interactional and relational; they are defined by both the organism(s) and their environment(s). 

A classic and still-relevant textbook illustration involves the so-called “peppered moth.” Until the Industrial Revolution, a "cryptic" (light-colored) species of the peppered moth (Biston betularia) predominated in the English countryside over a darker "melanic" form (Biston carbonaria). The mottled wing coloration of B. betularia provided camouflage from avian predators as the moths rested on the trunks of lichen-encrusted trees. The darker, melanic form obviously did not share this advantage. But as industrial soot progressively blackened the tree trunks in areas close to expanding industrial cities, the relative frequency of the two forms was reversed; the birds began to prey more heavily on the now more visible peppered moths (Kettlewell 1955, 1973).^99,100 

The question is, where in this example was natural selection "located?" The short answer is that natural selection encompassed the entire configuration of factors that combined to influence differential survival and reproduction. In this case, an alteration in the relationship between the coloration of the trees and the wing pigmentation of the moths, as a consequence of industrial pollution, was an important proximate factor. But this factor was important only because of the inflexible resting behavior of the moths and the feeding habits and perceptual abilities of the birds. Had the moths been subject only to insect-eating bats that use "sonar" to catch insects on the wing, rather than a visual detection system, the change in background coloration would not have been significant. Nor would it have been significant were there not genetically based patterns of wing coloration in the two forms that were available for "selection". (It should also be noted that a subsequent challenge to Kettlewell’s methods and the validity of his findings was resolved when a British geneticist, Mike Majerus, undertook a study that confirmed the original results.) See Chris Hurley and Stephen Montgomery (2009)¹⁰¹ “Peppered Moths & Melanism.” (I Thank Dick Vane-Wright for this information.)  

Accordingly, the ongoing survival challenge (again, Darwin referred to it as “the struggle for existence”) imposes a potential constraint on all aspects of the process of living. Every feature, or trait, of a given organism can be viewed in terms of its relationship (for better or worse, or not at all) to this fundamental, built-in, inescapable problem. Accordingly, natural selection differentially favors proximate functional “means” over time that serve the ultimate biological “end” of survival and reproduction. Indeed, the very term “adaptation” is commonly defined as a feature that advances some process or deals with some challenge related to survival and reproduction.    

The Neo-Darwinian definition also tends to equate natural selection and evolution with genetic changes, rather than viewing evolution more expansively as a multileveled 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 (for example, in predator-prey interactions or between symbionts).^102,103 The rise of "multi-level selection theory" in biology during the past three decades has served as a helpful corrective to classic Neo-Darwinism.^104-106 So, also is the extensive work on “niche construction theory,”^107-109 as well as the growing literature on the role of cultural influences in evolution, culminating in humankind.^8,110-118 

Another way of framing it is that evolution involves four distinct categories of functional variation (1) molecular-genetic variation, (2) phenotypic variation (inclusive of developmental, physiological, and behavioral/cultural variations), (3) ecological (environmental) variations and (4) differential survival and reproduction as an outcome of the specific organism-environment relationships and interactions in a given context. Furthermore, the causal arrows between these domains can go in both directions.   

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 behavior that results in a new organism-environment relationship. In fact, a whole sequence of changes may ripple through a pattern of relationships. For instance, a climate change might alter the ecology, which might prompt a behavioral shift to a new habitat, which might encourage an alteration in nutritional habits, which might precipitate changes in the interactions among different species, resulting ultimately in the differential survival and reproduction of organisms with differing morphological characters and the genes that support them. 

An in vivo illustration of this causal dynamic can be found in the long-running research program in the Galápagos Islands among "Darwin's finches".¹¹⁹ It is well known that birds often use their beaks as tools, and that their beaks tend to be specialized for whatever food sources are available in a given environment. In the Galápagos Islands, the zoologist Peter Grant and his wife and colleague have observed many changes over the years among its fourteen closely related finch species in response to environmental changes.^120-123 During drought periods, for instance, small seeds become scarce, and the most abundant food source consists of much larger, tougher seeds that must be cracked open to get at their kernels. Birds with larger, stronger beaks have a functional advantage, and this is the proximate cause of their differential survival during a drought.   

In essence, then, natural selection is focused on the functional causes of differential survival and reproduction (the bioeconomics), and it is agnostic about how and why this has occurred in any given context. Contrary to Mayr, the survival imperative can indeed be posited as an overarching goal in living systems (without any scare quotes or “as ifs”), inclusive of the proximate teleonomic phenomena that are, in fact, causal influences in natural selection. The basic unit of analysis in this alternative paradigm is not the genes but interdependent living “systems” and their parts -- along with their external “affordances” and dependencies.^{8,9,47,48,83,92,124-130}A living system represents a “combination of labor” with an overarching vocation, a means-ends teleonomy. Some theorists¹³¹ have adopted the term “holobiont” to characterize this frame shift.

Lamarckism in Evolution

As noted earlier, some contemporary theorists have adopted the concept of “agency” to characterize this defining biological characteristic[1].^47,48 

Other theorists have adopted Humberto Maturana and Francisco Varela’s concept of “autopoiesis”.¹³⁰ Agency is a term that is utilized in biology to characterize the ability of a living system to act as an autonomous, self-directed agent – to vary its behavior and its environment “purposefully” in relation to external or internal (“physiological”) conditions and goals. When a persistent wolf chases an evasive hare, both are exercising agency -- not God’s will, or a philosophical concept but an evolved capability for meeting their needs and coping with challenges in their environments. Agency in living systems is a product of an evolutionary “trial and success” process, as Dobzhansky (1977) memorably put it.⁴⁴ 

For the record, the importance of the organism as a self-organized and self-directed agent in evolution can be traced back at least to Jean Baptiste de Lamarck, who proposed that changes in an animal’s “habits”, stimulated by environmental changes, have been a primary source of evolutionary change over time. Lamarck (1984/1809:114)¹³² 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 over the course of time controlled … the faculties which it possesses.” Darwin was open to Lamarck’s idea, calling it the “use and disuse of parts,” and mentioned it no less than 12 times in The Origin of Species, (1968/1859).¹ Conversely, late in life Lamarck embraced a precursor of Darwin’s natural selection idea.⁹  

However, Darwin’s view of the relative importance of behavior as a causal influence in evolution was guarded and equivocal: "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."  

A “Darwinized” version of Lamarck’s insight, called “Organic Selection Theory” made a brief appearance at the end of the 19th century. The basic idea was that purposeful behavioral changes could alter the selective context for natural selection. But this proposal was soon overwhelmed and supplanted by “mutation theory” and the later work that led to the Modern Synthesis.¹¹⁵  
The idea that behavior is an influence in evolutionary change was tentatively reintroduced by the paleontologist George Gaylord Simpson (1953) under the neologism of the Baldwin Effect.¹³³ However, he portrayed it as being of only minor significance in evolution.

A more direct challenge to the gene-centered Modern Synthesis came from the embryologist and geneticist Conrad Waddington,^134-138 who challenged the mainstream dogma when he produced experimental evidence for a Darwinized version of the Lamarckian theory of the inheritance of acquired characters that he called "genetic assimilation.” Waddington showed that certain developmentally influenced behavioral characters, like 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-centered view of evolution. As he pointed out, "it is the animal's behavior 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”.¹³⁸  

A theoretical turning point came with the major conferences and edited volume on Behavior and Evolution.⁴⁶ In a landmark follow-up essay on the subject, Mayr (1960)¹³⁹ concluded: “It is now quite evident that … the evolutionary changes that result from adaptive shifts are often initiated by a change in behavior, to be followed secondarily by a change in structure … Changes of evolutionary significance are rarely, except on the cellular level, the direct results of mutation pressure … The selection pressure in favor of the structural modification is greatly increased by a shift to a new ecological niche, by the acquisition of a new habit, or by both.” Mayr did not mention Lamarck, but he characterized these Lamarckian behavioral innovations as the “pacemakers” of evolution. (Mayr’s assertion in 1960 also seems to contradict the contrary view that he expressed in his 1961 Science paper).⁵⁴

 

Behavior and Evolution

In fact, the “purposeful” behavior of living organisms has had a major influence in shaping natural selection and the trajectory of evolution over time. It could be said – with Dobzhansky – that the behavior of living organisms exhibits an internal, or natural teleology. The term highlights the fact that evolved teleonomic processes and systems can exert a significant causal influence on the properties and actions of living systems, both in themselves and in others.¹⁴⁰ Some theorists speak of “agency”; others of “autopoiesis” (or self-maintenance); still others of “cybernetic” (feedback-driven) goal-directedness. The “ultimate” evolutionary consequences of this dynamic could be characterized as “teleonomic selection.⁹”  

A well-documented illustration involves the remarkable tool-using behavior of the so-called woodpecker finch. Cactospiza pallidus is one of the fourteen 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 skillfully 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 digging "tools" of the right size, shape and strength and carrying them from tree to tree.^119,141 

What is most significant about this distinctive behavior, for our purpose, is the "downward" effect it has had 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. But C. pallidus has no such anatomical modification. In other words, the invention of a digging tool enabled the woodpecker finch to circumvent the requirement for an otherwise necessary morphological change. This behavioral “workaround” in effect provided both a facilitator and a selective shield, or mask. (For a more recent example of social behavior as a facilitator of genetic change, see Shell, et al., 2021.)¹⁴² 

Indeed, we now know that behavioral innovations by living organisms are ubiquitous in the natural world. Some of them are legendary. One of the most frequently cited examples concerns the discovery in the late 1940s that British blue tits had developed the clever habit of prying open the foil caps from the milk bottles that, in those days, were delivered directly to customers’ front stoops.^143,144 Also legendary is psychologist Wolfgang Köhler's experiments with chimpanzees in the 1920s. In one case, captive chimpanzees were able to solve the problem of how to reach bunches of bananas that were suspended high overhead by stacking wooden boxes on top of one another to create a makeshift ladder.^44,145 Especially compelling is the example of Imo, the young female in a Japanese macaque colony, because this inventive monkey devised two novel food-processing techniques that subsequently spread to other members of her troop.¹⁴⁶ Likewise, primatologist Jane Goodall observed many examples of novel behaviors among the chimpanzees she studied at Gombe Stream in Tanzania.¹⁴⁷ Also famous are the experiments by the Nobel Prize-winning entomologist Karl von Frisch on learning in honeybees.^144,148 Honeybees are also good problem solvers.^149,150  

It is also frequently the case that the teleonomic behavioral choices of one species can become the instrument of natural selection in another species. One example among many can be found in the rainforest of the Olympic National Park, in the state of Washington, where 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 low sunlight conditions of the park. However, it is the Sitka spruce that dominate, 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 preferences of the elk are the “proximate cause” of differential survival between the hemlock and spruce trees.

Mind in Evolution

Over the past half century, the research on learning and innovation by 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 songbirds, hens, rats, gorillas, chimpanzees, elephants, dolphins, whales and many others. (In the index to their book on Animal Traditions, Eytan Avital & Eva Jablonka, 2000, list well over 200 different species.)¹⁵¹ 

We now know that primitive E. coli bacteria, slime molds, 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.  

Our respect for the "cognitive" abilities of various animals also continues to grow.^44,152 Innumerable studies have documented that many species are capable of sophisticated cost-benefit calculations, sometimes involving several variables, including the 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. Many of these decisions are under tight genetic control, with "pre-programmed" selection criteria. But many more are also, at least in part, the product of experience, trial-and-error learning, observation and even, perhaps, some insight learning.^9,115 One classic illustration is ethologist Bernd Heinrich’s experiments in which naïve ravens quickly learned to use their beaks and claws to pull up “fishing lines” hung from their roosts, in order to capture the food rewards attached at the ends.¹⁵³ (Heinrich’s 1999 book, The Mind of the Raven, provides extensive evidence for the mental abilities of these remarkable birds.)¹⁵⁴  

Indeed, even plants make “decisions”. In the marine alga Fucus, for example, biologists Simon Gilroy and Anthony Trewavas (2001)¹⁵⁵ have found that at least 17 environmental conditions can be “sensed”, and the information that it collects is then either summed or integrated synergistically as appropriate. Gilroy and 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.”¹⁵⁶ 

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 instance, red-wing blackbirds, which readily colonize new habitats, are especially prone to acquire new food habits -- or food aversions -- from watching other birds.¹⁵⁷ Pigeons can learn specific food-getting skills from other pigeons.¹⁵⁸ Domestic cats, when denied the ability to observe conspecifics, will learn certain tasks much more slowly or not at all.¹⁵⁹ And, 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.¹⁶⁰ 

True "imitation" (including the learning of motor skills) has also been observed in (among 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 behaviors, including grooming, sleeping postures, even mimicking the divers that scraped the observation windows of their pools, down to the sounds made by the divers' breathing apparatus).¹¹⁵ 

Not surprisingly, the most potent cognitive skills have been found in social mammals, especially the great apes. They display intentional behavior, planning, social coordination, understanding of cause and effect, anticipation, generalization, even deception. Primatologists Richard Byrne and Andrew Whiten, in their two important edited volumes on the subject, refer to it as "Machiavellian intelligence.”^160-162 Cognitive skills and social learning have provided a powerful means -- which humankind has greatly enhanced -- for accumulating, dispersing and perpetuating novel adaptations without waiting for slower-acting genetic changes to occur. 

Tool-use is an especially significant and widespread category of adaptive behavior 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)¹⁶³ pointed out in his comprehensive survey and synthesis, Sociobiology, tools provide a means for quantum jumps in behavioral invention, and in the ability of living organisms to manipulate their environments. Tool-use results in otherwise unattainable behavioral outcomes (synergies).^163-165 

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".^163-166 Not only are chimpanzees proficient as tool-users but they can also make tools. They break off small tree branches and strip them to fabricate ant "wands"; they use their bodies for leverage when they break down larger sticks to make hammers; they work leaves into sponges; and they carefully select stones of the right size and shape for the job at hand and will then carry them to their worksites. 

Finally, it is important to emphasize the role of “culture” and cultural transmission in evolutionary change. The debate about the role of culture in other species, like chimpanzees, may still be unresolved, but there can be no doubt that behavioral and cultural evolution played an important role in human evolution.^{7,9,110-113,117,167,168,170,172} 

Biologist Richard Dawkins, in his popular book, The Selfish Gene, characterized living systems, like humankind, as “survival machines – robot vehicles that are blindly programmed to preserve the selfish molecules known as genes” (Dawkins, 1989/1976: ix).⁵ We now know that this is definitely not the case. Arguably, it is the other way around; the genes have evolved in the service of living organisms, for the most part, and the exceptions prove the rule. 

 

The “Synergism Hypothesis” Revisited

A major theoretical issue in mainstream evolutionary biology over the past two decades has concerned the rise of complexity over time, and a search has been underway for “a Grand Unified Theory” – as biologist Daniel McShea (2015) characterized it – that is consistent with Darwin’s great vision. McShea aspired to identify “some single principle or some small set of principles” that could explain the evolutionary trend toward greater complexity.” Likewise, biologist Deborah Gordon (2007) noted that: “Perhaps there can be a general theory of complex systems, but we don’t have one yet.¹⁷⁴”  

As it happens, such a theory does exist. It was first proposed in The Synergism Hypothesis: A Theory of Progressive Evolution,⁶ and it involves an economic (or perhaps bioeconomic) theory of complexity. Simply stated, cooperative interactions of various kinds, however they may occur, can produce novel combined effects – synergies – with functional advantages that may, in turn, become direct causes of natural selection. The focus of the Synergism Hypothesis is on the favorable selection of synergistic “wholes” and the combination of genes that produces these wholes. The parts (and their genes) that produce these synergies may, in effect, become interdependent units of evolutionary change.  

In other words, the Synergism Hypothesis is a theory about the unique combined effects produced by the relationships between things. We refer to it as Holistic Darwinism because it is entirely consistent with natural selection theory, properly understood. It is the functional (economic) benefits associated with various kinds of synergistic effects in any given context that are the underlying causes of cooperative relationships – and of complex organization – in the natural world. The synergy produced by the whole provides the proximate functional payoffs that may differentially favor the survival and reproduction of the parts, and their genes.^7-9,167  

Although it may seem like backwards logic, the thesis is that functional synergy is the cause of cooperation and complexity in living systems, not the other way around. To repeat, the Synergism Hypothesis is basically an economic theory of emergent complexity, and it applies equally to biological and cultural evolution – most notably in humankind. Indeed, it now appears that social cooperation has been a key to our evolution as a species, and that social synergy is the reason why we cooperate. In a very real sense, we invented ourselves.⁹ 

It should also be stressed that the synergies can very often be quantified. A legendary example among many others⁹ is the way emperor penguins huddle closely together in large colonies, sometimes numbering in the tens of thousands, to share heat during the bitterly cold Antarctic winter. In so doing, they are able to reduce their individual energy expenditures by 20 to 50 percent, depending upon where they are in the huddle and the wind direction and speed.¹⁷⁵  

The biologists John Maynard Smith and Eörs Szathmáry (1995, 1999),^175,176 in their path-breaking work on the “major transitions” in evolution, came to the same conclusion independently about the causal role of synergy in evolution – although they graciously acknowledged the priority of my 1983 book in one of their two books on the subject. They applied their version of the Synergism Hypothesis specifically to the problem of explaining the emergence of new levels of biological organization over time.¹⁷⁷ Maynard Smith¹⁷⁸ also proposed the concept of Synergistic Selection as (in effect) a sub-category of natural selection. Synergistic Selection refers to the many contexts in nature where two or more genes/genomes/individuals have a shared fate; their combined effects are functionally interdependent.  

Thus, cooperative phenomena of various kinds, which are portrayed as being highly constrained and problematic under the predominately competitive assumptions of the Modern Synthesis, are now seen to play an important causal role in living systems, and in evolution. Biologist Richard Michod (1999)¹⁷⁹ asserts that “cooperation is now seen as the primary creative force behind ever greater levels of complexity and organization in all of biology.” And Martin Nowak¹⁸⁰ calls cooperation “the master architect of evolution.” However, it is not cooperation per se that has been the “creative force” or the “architect”. Rather, it is the unique combined effects (the synergies) produced by cooperation. Beneficial synergies of various kinds have been a prodigious source of evolutionary novelties and the underlying cause of cooperation and increased complexity in evolution over time.^5,8,9,167 

Defining Complexity

The basic question, therefore, is what are the advantages of biological complexity? However, there is also a prior question: What is “complexity”? One must start by defining what the term complexity means in relation to living systems before examining how – and why – biological complexity has evolved over time. 

The issue of how to define biological complexity has been much debated over the years, and it is evident that there is no one correct way to measure it; it can be defined in different ways for different purposes. However, two alternative methodologies are relevant (at least in theory) as ways of characterizing the broad evolutionary trend toward multi-leveled complex systems over the past 3.8 billion years or so, beginning with the origins of life and culminating (temporally at least) in humankind.  

One method is structural. A synthetic complexity scale can be constructed from the number of levels of organization (inclusive of social organization), the number of distinct “parts”, the number of different kinds of parts, and the number of interconnections among the parts. The other method is functional. A complexity scale can be derived from the number of functionally discrete “tasks” in the division/combination of labor at all levels of organization, coupled with the quantity of “control information” that is generated and utilized by the system. Control information is defined as “the capacity to control the capacity to do work” in a cybernetic process; it is equivalent to the amount of thermodynamic work that a system can perform. Both of these methodologies are relevant here. 

There are also various ways of measuring the economic costs and benefits of biological complexity. The “ultimate” measure is, of course, reproductive success. Although the level of personal investment can vary widely in the natural world, an organism must sustain a minimal “economic profit” in order to be able to reproduce itself, and the more offspring it produces the more profitable it is from an ultimate evolutionary perspective.  

However, there are also a many other “proximate” ways of measuring the costs and benefits involved in “earning a living” in nature, and a number of familiar economic criteria are likely to have been important from a very early stage in the history of life on Earth – capital costs, amortization, operating costs and, most especially, strict economic profitability. The returns had to outweigh the costs. There is, of course, a large research literature and various journals in behavioral ecology and bioeconomics that are focused on just such proximate issues. 

Consider the fundamental need for energy capture. Dating back to physicist Erwin Schrӧdinger’s book, What is Life? in 1944,¹² it has long been appreciated that thermodynamics is of central importance in understanding the nature of life, and the challenges of living. Living systems must do work and are subject to thermodynamic entropy and the Second Law. This imposes significant functional requirements. However, there is also a deep tradition in biophysics that assumes away the economic challenges involved in creating “negative entropy” (Schrӧdinger’s neologism). Indeed, there is a school of theorists who have advanced the proposition that energy is somehow a free good and that available energy itself “drives” the process of creating order and organization in the living world.¹⁸¹ 

A famous experiment in physics, Maxwell’s Demon, unwittingly demonstrated why this assumption is incorrect. In a nutshell, there is no way the Demon could create thermodynamic order “without the expenditure of work” (to use Maxwell’s own, ill-considered claim for the Demon). Living systems must adhere to the first and only law (so far) of “thermoeconomics”, namely, that the energetic benefits (the energy made available to the system to do work) must outweigh the costs required for capturing and utilizing it. From the very origins of life, energy capture and metabolism have played a key role. As biological complexity has increased over time, the work required to obtain and use energy to sustain the system has increased correspondingly. Indeed, improvements in bioenergetic technologies represent a major theme in evolutionary history and, in every case, involved synergistic phenomena. 

Much of the work in complexity science in recent years has been focused on the physical, structural, functional, and dynamical aspects of complex phenomena. However, complex living organisms are distinctive in that they are also subject to basic economic criteria, and to economic constraints. Biological complexity is not simply an historical artifact, much less the product of some exogenous physical trend, force, or “law”. Over the years, many candidate laws have been proposed that have claimed to explain complexity in evolution, going back to Jean Baptiste de Lamarck, and to Herbert Spencer’s “universal law of evolution” during the Nineteenth Century. In the latter part of the Twentieth Century, the development of new mathematical tools and rise of complexity theory in various disciplines inspired a plethora of new law-like, or mechanistic explanations.¹⁸² This theme has continued into the new century, as documented in detail in Corning (2018).⁹  

The problem with all such deterministic theories is that they explain away the very thing that needs to be explained – namely, the contingent nature of living systems and their fundamentally functional, adaptive properties. As the biologist Theodosius Dobzhansky long ago (1977) pointed out: “No theory of evolution which leaves the phenomenon of adaptation an unexplained mystery can be satisfactory.” The purveyors of these theories often seem oblivious to the inescapable challenges associated with Darwin’s “struggle for existence” in the natural world, and they discount the economics – the costs and benefits of complexity. Nor can they explain the fact that some 99 percent of all the species that have ever evolved are now extinct. Life is a phenomenon that is at all times subject to the requirement that the bioeconomic benefits (direct or indirect) of any character or trait – including complexity -- must outweigh the costs. It is subject to functional criteria and the calculus of economic costs and benefits in any given environmental context.

Synergistic Selection

As noted earlier, biologist John Maynard Smith proposed the concept of Synergistic Selection in a 1982 paper as (in effect) a sub-category of natural selection. Synergistic Selection refers to the many contexts in nature where two or more genes/genomes/ parts/individuals have a shared fate; they are functionally interdependent. Maynard Smith illustrated with a formal mathematical model that included a term for “non-additive” benefits (when 2+2=5). The idea is also distilled in the catchphrase “the whole is greater than the sum of its parts,” which traces back to the Metaphysics of Aristotle (ca. 350 B.C., Book H, 1045: 8-10).  

However, Synergistic Selection is an evolutionary dynamic with much wider scope even than Maynard Smith envisioned. It includes, among other things, many additive phenomena with combined threshold effects and, more important, many “qualitative novelties” that cannot even be expressed in quantitative terms. There are, in fact, many kinds of synergies. Synergistic Selection focuses our attention on the causal dynamics and selective outcomes when synergistic effects of various kinds arise in the natural world. The claim is that synergy, and Synergistic Selection, has driven the evolution of cooperation and complexity in living systems over time, including especially the major transitions in evolution.  

One example (among the many cited in Corning (2018)⁹ is the evolution of eukaryotes. Increased size and complexity can have many functional advantages in the natural world, and eukaryotic cells, inclusive of their complex internal architecture, are on average some 10-15,000 times larger than the typical prokaryote. However, this huge size difference requires many orders of magnitude more energy, and the key to solving this functional imperative was a symbiotic (synergistic) union between an ancestral prokaryote and an ancestor of the specialized, energy producing mitochondria in modern eukaryotic cells. Not only was this potent new combination of labor mutually beneficial for each of the two partners but it created a pathway for expanding and multiplying those benefits many times over. Some specialized cells in complex organisms like humans may contain hundreds, or even thousands, of mitochondria. Liver cells, for instance, have some 2,500 mitochondria and muscle cells may have several times that number. To repeat, it could be called a “synergy of scale.” 

Many things can influence the likelihood of cooperation and synergy in the natural world – the ecological context, specific opportunities, competitive pressures, the risks (and costs) of cheating or parasitism, effective policing, genetic relatedness, biological “pre-adaptations”, and especially the distribution of bioeconomic costs and benefits. However, an essential requisite for cooperation (and complexity) – is functional synergy. Just as natural selection is agnostic about the sources of the functional variations that can influence differential survival and reproduction, so the Synergism Hypothesis is agnostic about how synergistic effects can arise in nature. They could be self-organized; they could be a product of some chance variation; they could arise from a happenstance symbiotic relationship; or they could be the result of a purpose-driven behavioral innovation by some living organism. 

It should also be stressed that there are many different kinds of synergy in the natural world, including (as noted above) synergies of scale (when larger numbers provide an otherwise unattainable collective advantage), threshold effects, functional complementarities, augmentation or facilitation (as with catalysts), joint environmental conditioning, risk- and cost-sharing, information-sharing, collective intelligence, animal-tool “symbiosis” and, of course, the many examples of a division of labor (or more accurately, a “combination of labor”). Indeed, many different synergies may be bundled together (a synergy of synergies) in a complex socially organized “superorganism” like leaf cutter ants, or Homo sapiens. 

It should also be noted that size has played a critically important role in evolution, and that there is a close linkage between size and biological complexity, as discussed in depth by biologist John Tyler Bonner in his book, Why Size Matters (2006).¹⁸³ However, size is not an end in itself. It arises because it confers various functional advantages – various synergies of scale. These may include such things as improved mobility, more effective food acquisition, efficiencies in energy consumption, more efficient and effective reproduction, and, not least, protection from predators. 

Consider the example of volvocines, a primitive order of aquatic green algae that form into tight-knit colonies resembling integrated organisms. One of the smallest of these colonies (Gonium) has only a handful of cells arranged in a disk, while the Volvox that give the volvocine line its name may have some 50-60,000 cells arranged in the shape of a hollow sphere that is visible to the naked eye. Each Volvox cell is independent, yet the colony-members collaborate closely. For instance, the entire colony is propelled by a thick outer coat of flagella that coordinate their exertions to keep the sphere moving and slowly spinning in the water – in other words, a synergy of scale. 

Some of the synergies in the Volvox were documented in a study many years ago by Graham Bell (1985),¹⁸⁴ and in more recent studies by Richard Michod (1999).¹⁷⁹ The largest of the Volvox colonies have a division of labor between a multi-cellular body and segregated reproductive cells. Bell's analyses suggested some of the benefits. A division of labor and specialization facilitates growth, resulting in a much larger overall size. It also results in more efficient reproductive machinery (namely, a larger number of smaller germ cells). The large hollow enclosure in Volvox also allows a colony to provide a protective envelope for its daughter colonies; the offspring disperse only when the parental colony finally bursts apart. 

But there is one other vitally important synergy of scale in Volvox. It turns out that their larger overall size results in a much greater survival rate than in the smaller Gonium. The volvocines are subject to predation from filter feeders like the ubiquitous copepods, but there is an upper limit to the prey size that their predators can consume. The larger, integrated, multi-cellular Volvox colonies are virtually immune from predation by these filter feeders. 

The Synergism Hypothesis can also account for the unique trajectory of human evolution, including the transformative influence of cultural evolution. Synergistic behavioral and cultural innovations played a key role at every stage in the process. (There are three chapters concerned with this thesis in my 2018 book, on Synergistic Selection: How Cooperation Has Shaped Evolution and the Rise of Humankind.) It can also help to explain warfare in human societies, as elsewhere in the natural world. Among other things, warfare is a highly synergistic phenomenon. 

The Synergism Hypothesis also encompasses the role of both “positive” and “negative” synergies and their selective consequences for a given organism, group, or species. One obvious example is how organized, cooperative predation may be viewed very differently by a group of predators and their prey. Another example is how individuals and business corporations in human societies may benefit in various ways from burning fossil fuels, yet their combined actions also produce global warming (a negative synergy of scale). It should also be noted that Synergistic Selection is a dynamic that occurs at both the “proximate” (functional) level and at the “ultimate” evolutionary level. Indeed, proximate synergies are in many cases the direct cause of differential survival and reproduction over time. Some predator-prey interactions are, again, a canonical example. 

The Synergism Hypothesis also offers an explanation for the ubiquitous role of cybernetic “control” processes in living systems at all levels. (In humankind, we refer to it, variously, as “management”, “politics”, and “governance”.) As Maynard Smith and Szathmáry (1995; 1999) show in detail in their two books on the major transitions in evolution, every new form of organization in the natural world represents a distinct “combination of labor” that requires integration, coordination, and regulation/policing. From eukaryotic protists to Adam Smith’s famous pin factory and the emerging global society in humankind, cybernetic governance is a central challenge and a necessary concomitant. 

The historical process through which multilevel biological systems have evolved over time can be framed as a sequence of major transitions in complexity – from the very origins of life itself to the emerging global society that humankind is now engaged in creating (for better or worse). And, at every level in this hierarchy, we can see the driving influence of synergy and Synergistic Selection. From an evolutionary/biological perspective, complexity has a purpose – or perhaps even many. In any case, biological complexity must ultimately pass the test of being useful for survival and reproduction. Cooperation may have been the vehicle, but synergy was the driver.

The Physics of Evolution

We should also note that there has been a long-standing face-off between physicists, who have intruded into biology in various ways over the years, and the biologists who claim that biological phenomena are distinctive and go beyond physics. (See the extended review in Philip Ball, “Why Physics is Not a Discipline,” Nautilus, April 18, 2015.) Actually, both sides are partly correct. As we have noted, living systems are distinctive in being evolved, contingent thermodynamic systems that have also been shaped by, and depend upon, their variable natural environments. Physicists do not understand and cannot explain the fundamental biological concept of “teleonomy”. On the other hand, what biologists consider as parts of the “natural environment” include many of the physical forces/processes that physicists study/measure. An obvious example is gravity, which has influenced biological evolution in many ways. Consider the evolution of birds.¹⁸⁵ Or consider water. Or consider our oxygenated atmosphere. Or our variable air temperatures. The evolved functional designs in living systems represent various “purposeful” ways of adapting to these conditions. If there is a physics of biology, there is also a biology of physics. 

Conclusion: An “Inclusive Synthesis”

The Nobel physicist Albert Einstein long ago observed that “a theory is all the more impressive the greater is the simplicity of its premises, the more different are the kinds of things it relates and the more extended its range of applicability.”⁹ I believe it is both possible and appropriate to reduce fundamental aspects of the evolutionary process, in nature and human societies alike, to a unifying theoretical framework. Like the concept of natural selection itself, the label “Inclusive Synthesis” involves an “umbrella term” (an open-ended category) that identifies a common set of causal influences across a very diverse array of phenomena. It focuses our attention on the causal role that living systems themselves and their functional synergies have had at every step in the evolution of biological complexity, beginning with the origins of life itself.  

Many theorists these days are calling for a new post-modern, post-neo-Darwinian evolutionary synthesis. Some theorists advocate the adoption of a more elaborate “multilevel selection” model.¹⁰⁴ Others speak of an “Extended Evolutionary Synthesis” (Pigliucci and Müller) that would include developmental processes and Lamarckian inheritance mechanisms, among other things. Biologist Denis Noble (2015) has proposed what he calls an “Integrative Synthesis” that would include the role of physiology in the causal matrix.⁸²  

It is clear that a much more inclusive framework is needed, one that captures the full dynamics and interactions among the many different causal influences at work in the natural world. We also need to view the evolutionary process in terms of multi-leveled systems – functional organizations of matter, energy, and information, from genomes to ecosystems. And we must recognize that the level of selection – of differential survival and reproduction – in this hierarchy of system levels is determined in each instance by a synergistic configuration, or network of causes. Indeed, the outcome in any given context may be a kind of vector sum of the causal forces that are at work at several different levels at once. 

What is needed going forward is a broadly ecumenical paradigm that would provide more of a work plan than a finished product. I call it an “Inclusive Synthesis.” It is an open-ended framework for explaining how, precisely, natural selection “does its work” in any given context (what causal factors influence adaptive changes). It would also represent an ongoing work-in-progress rather than a completed theoretical edifice. 

Indeed, we must also use our growing understanding of the evolutionary process – especially our insights into the role of teleonomy (‘agency”) and the centrality of cooperative effects (synergies) – to address the at-risk future of life on Earth. For our species is increasingly in peril.

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