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Agency in Evolutionary Biology

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Abstract

Evolutionary biology has been criticised by Karl Popper, Denis Noble and others for reasons that can be grouped into two fundamental sources of disagreement. First, there is the idea of organisms as indeterminate (or ‘free’) problem-solvers that control their own evolutionary fate by choosing their niche. Herein fall the majority of Popper’s ideas about ‘active’ and ‘passive’ Darwinism, the critique of natural and sexual selection, the philosophy of indeterminism and how biology is irreducible to chemistry—which is conserved in Noble’s critique. Second, there is the idea that evolutionary theory should not give a privileged role to DNA in its explanations—which has been extended by Noble in the spirit of Popper’s argument. I propose that these two fundamental sources of disagreement are two sides of the same coin—which is, namely, evolutionary biology’s concept of the agency. In this light, the former is the construction of Popper/Noble’s particular concept of agency, whilst the latter is an attack on evolutionary biology’s concept of agency. Here I argue that although some of the disagreement is superficially about use-of-language, there is a more fundamental problem about the philosophical foundations of incompatible concepts of agency in scientific traditions stemming from rationalism and empiricism.

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Notes

  1. 1.

    The point I want to make now is that all attempts to answer that question [evolution, especially of humans] before 1859 are worthless and that we will be better off if we ignore them completely” (Simpson 1966, p. 1).

  2. 2.

    This description is a chapter heading of Huxley’s (1942) The Modern Synthesis.

  3. 3.

    There are numerous books that frame the question of adaptation within a pre-Darwinian historical context, which trace adaptationist thinking back to the Ancient Greeks (Bowler 1983; Riskin 2016; Stott 2012), especially Aristotle who is even accredited by Darwin (1859) in later editions of The Origin of Species.

  4. 4.

    I am using this term to refer particularly to the philosophical perspective epitomised by David Hume. These views differ from what John Locke referred to as ‘continental rationalism’, which is equally epitomised by Rene Descartes. ‘British empiricism’ is a contemporary term, which I use following (Godfrey-Smith 1996).

  5. 5.

    If an account must be given of the contrivance which we observe; if it be demanded, whence arose either the contrivance by which the young animal is produced, or the contrivance manifested in the young animal itself, it is not from the reason of the parent that any such account can be drawn. He is the cause of his offspring in the same sense as that in which a gardener is the cause of the tulip which grows upon his parterre, and in no other. We admire the flower; we examine the plant; we perceive the conduciveness of many of its parts to their end and office; we observe a provision for its nourishment, growth, protection, and fecundity; but we never think of the gardener in all this. We attribute nothing of this to his agency; yet it may still be true, that without the gardener we should not have had the tulip: just so it is with the succession of animals even of the highest order. For the contrivance discovered in the structure of the thing produced, we want a contriver. The parent is not that contriver. His consciousness decides that question. He is in total ignorance why that which is produced took its present form rather than any other. It is for him only to be astonished by the effect” (Paley 1802, p. 34).

  6. 6.

    One of the most remarkable features in our domesticated races is that we see in them adaptation, not indeed to the animal’s or plant’s own good, but to man’s use or fancy. … we must, I think, look further than to mere variability. We can not suppose that all the breeds were suddenly produced as perfect and as useful as we now see them; indeed, in many cases, we know that this has not been their history. The key is man’s power of accumulative selection: nature gives successive variations; man adds them up in certain directions useful to him. In this sense he may be said to have made for himself useful breeds. The great power of this principle of selection is not hypothetical. It is certain that several of our eminent breeders have, even within a single lifetime, modified to a large extent their breeds of cattle and sheep. In order fully to realise what they have done it is almost necessary to read several of the many treatise devoted to this subject, and to inspect the animals” (Darwin 1859, p. 23–24).

  7. 7.

    All major evolutionary theories before Darwin, and nearly all important versions that followed his enunciation of natural selection as well, retained fealty to an ancient Western tradition, dating to Plato and other classical authors, by presenting a fundamentally “internalist” account, based upon intrinsic and predictable patterns set by the nature of living systems, for development or “unfolding” through time” (Gould 2002, p. 160).

  8. 8.

    As the student proceeds from his freshman course to and through his doctoral dissertation, the problems assigned to him become more complex and less completely precedented. But they continue to be closely modelled on previous achievements as are the problems that normally occupy him during his subsequent independent scientific career. One is at liberty to suppose that some—where along the way the scientist has intuitively abstracted rules of the game for himself, but there is little reason to believe it. Though many scientists talk easily and well about the particular individual hypotheses that underlie a concrete piece of current research, they are little better than laymen at characterizing the established bases of their field, its legitimate problems and methods. If they have learned such abstractions at all, they show it mainly through their ability to do successful research. That ability can, however, be understood without recourse to hypothetical rules of the game” (Kuhn 1962, p. 47).

  9. 9.

    This respect can be seen in Darwin’s ‘major funeral’ in Westminster Abbey, where he was honoured more as a public intellectual than as the father of evolutionary biology (Bowler 1984; Desmond and Moore 1991; Gould 1978; Mayr 1982).

  10. 10.

    Suppose, for example, that a group of distinguished families possess potential or actual versatility to the extent of being able successfully to fill the role, either of a landed gentleman administering his estates, or of a soldier. A is the eldest son, and stays at home; his brother B goes to the wars; then so long as A has some eight children, it does not matter, genetically, if B gets killed, or dies childless, there will be nephews to fill his place” (Fisher 1914, p. 315).

  11. 11.

    Williams’ [1966] shift in emphasis from individuals to genes went almost unnoticed. His interpretation has not only peacefully coexisted with the synthetic theory for two decades, but has also been typically regarded as a brilliant defence of it. Williams’ genic selection, however, has taken on a new-found importance. When genic selection was contrasted with selection on populations, it drew little attention, as most people mentally equated genic selection with individual selection. However, with the publication of Richard Dawkins’s The Selfish Gene, genic selection was pitted against individual selection. In Dawkins’s work, the significance of Williams’ seemingly subtle shift in emphasis became focused and clearly associated with a fundamental shift in the language of evolution” (Buss 1987, p. 175).

  12. 12.

    I hope that this book will help to purge biology of what I regard as unnecessary distractions that impede the progress of evolutionary theory and the development of a disciplined science for analysing adaptation” (Williams 1966, p. 4).

  13. 13.

    The decision as to the purpose of a mechanism must be based on an examination of the machinery and an argument as to the appropriateness of the means to the end” (Williams 1966, p. 12).

  14. 14.

    The natural selection of phenotypes cannot in itself produce cumulative change, because phenotypes are extremely temporary manifestations” (Williams 1966, p. 23).

  15. 15.

    Was there to be any end to the gradual improvement in the techniques and artifices used by the replicators to ensure their own continuation in the world? There would be plenty of time for improvement. What weird engines of self-preservation would the millennia bring forth? Four thousand million years on, what was to be the fate of the ancient replicators? They did not die out, for they are past masters of the survival arts. But do not look for them floating loose in the sea; they gave up that cavalier freedom long ago. Now they swarm in huge colonies, safe inside gigantic lumbering robots, sealed off from the outside world, communicating with it by tortuous indirect routes, manipulating it by remote control. They are in you and in me; they created us, body and mind; and their preservation is the ultimate rationale for our existence. They have come a long way, those replicators. Now they go by the name of genes, and we are their survival machines” (Dawkins 1976, p. 19–20).

  16. 16.

    My primary intention [by introducing memes], however, was not to make a contribution to the theory of human culture, but to downplay the gene as the only conceivable replicator that might lie at the root of a Darwinian process. I was trying to push ‘Universal Darwinism’ (the title of a later paper, based on my lecture to the 1982 conference commemorating Darwin’s death). Nevertheless I am delighted that… others have run, so productively, with the meme ball” (Dawkins 2013, p. 280).

  17. 17.

    That cultural variants are not viewed as replicators is not universally agreed upon, but the argument on both sides has become dominated by what words imply. For example, those in favour of memes (e.g. Dennett 2017) cite those who are not in favour as supporting their argument (e.g. Richerson and Boyd 2005)—despite explicitly rejecting the term ‘meme’ because it implies that cultural variants are replicators. In general, I would favour the approach of Richerson and Boyd’s perspective because it explicitly acknowledges that the mechanism of cultural inheritance is critical to exactly what is being preserved (and does not loosely apply the replicator concept in the absence of a clear understanding of what is replicated).

  18. 18.

    If a genetic change that lengthens the bone also curves the eyebrow, then our adaptive explanation should recognise that; we should be interested in the genetic differences that give rise not merely to differences in toe-length but to differences in toe-length-plus-eyebrow-shape, even if eyebrow shape should turn out to be selectively neutral. This is an answer that would not have been obvious to the organism-centred view of classical Darwinism but comes readily to a theory that is gene-centred” (Cronin 1991, p. 107).

  19. 19.

    For my part, when I enter most intimately into what I call myself, I always stumble on some particular perception or other, of heat or cold, light or shade, love or hatred, pain or pleasure. I never can catch myself at any time without a perception, and never can observe any thing but the perception. When my perceptions are removed for any time, as by sound sleep, so long am I insensible of myself, and may truly be said not to exist. And were all my perceptions removed by death, and could I neither think, nor feel, nor see, nor love, nor hate, after the dissolution of my body, I should be entirely annihilated, nor do I conceive what is further requisite to make me a perfect nonentity. If any one, upon serious and unprejudiced reflection, thinks he has a different notion of himself, I must confess I can reason no longer with him. All I can allow him is, that he may be in the right as well as I, and that we are essentially different in this particular. He may, perhaps, perceive something simple and continued, which he calls himself; though I am certain there is no such principle in me” (Hume 1738, p. 134).

  20. 20.

    There is a doctrine about the nature and place of the mind which is prevalent among theorists, to which most philosophers, psychologists and religious teachers subscribe with minor reservations.… The official doctrine, which hails chiefly from Descartes, is something like this. With the doubtful exceptions of the mentally-incompetent and infants in arms, every human being has both a body and a mind. Some would prefer to say that every human being is both a body and a mind. The body and the mind are ordinarily harnessed together, but after the death of the body the mind may continue to exist and function. Human bodies are in space and are subject to mechanical laws which govern all other bodies in space. … But minds are not in space, nor are their operations subject to mechanical laws. … Such in outline is the official theory. I shall often speak of it, with deliberate abusiveness, as “the dogma of the Ghost in the Machine.” I hope to prove that it is entirely false, and false not in detail but in principle. It is not merely an assemblage of particular mistakes. It is one big mistake and a mistake of a special kind. It is, namely, a category mistake. … [p. 66] … In short, then, the doctrine of volitions is a causal hypothesis, adopted because it was wrongly supposed that the question, ‘What makes a bodily movement voluntary?’ was a causal question” (Ryle 1949, p. 17 and p. 66 as marked).

  21. 21.

    There is a thorough Neo-Darwinian discussion of epigenetics in Haig (2007).

  22. 22.

    These ideas are put forward by Cairns-Smith (1982), and enthusiastically discussed by Dawkins (1986). A more modern treatment is given by the seminal Maynard Smith and Szathmary (1995).

  23. 23.

    In my opinion, passive Darwinism turns out, when confronted by active Darwinism, to be a mistaken interpretation of the process of adaptation. Adaptation is, I suggest, essentially a trial and error learning process that extends over many generations. … [p. 121] … We should regard the whole of evolution as a huge learning process going in all sorts of directions and specialisations” (Popper 1986, in Niemann 2014, p. 120 and p. 121).

  24. 24.

    My general point is that there is one limiting constraint upon all speculations about life in the universe. If a life-form displays adaptive complexity, it must possess an evolution mechanism capable of generating adaptive complexity. However diverse evolutionary mechanisms may be, if there is no other generalization that can be made about life all around the Universe, I am betting it will always be recognizable as Darwinian life” (Dawkins 1983, in Bendall 1983, p. 423).

  25. 25.

    In like manner we say that the designer of all organisms is so incorporate with the organisms themselves—so lives, moves, and has its being in those organisms, and is so one with them—they in it, and it in them—that it is more consistent with reason and the common use of words to see the designer of each living form in the living form itself, than to look for its designer in some other place or person. Thus we have a third alternative presented to us. Mr. Charles Darwin and his followers deny design, as having any appreciable share in the formation of organism at all. Paley and the theologians insist on design, but upon a designer outside the universe and the organism. The third opinion is that suggested in the first instance, and carried out to a very high degree of development by Buffon. It was improved, and, indeed, made almost perfect by Dr. Erasmus Darwin, but too much neglected by him after he had put it forward. It was borrowed, as I think we may say with some confidence, from Dr. Darwin by Lamarck, and was followed up by him ardently thenceforth, during the remainder of his life, though somewhat less perfectly comprehended by him than it had been by Dr. Darwin. It is that the design which has designed organisms, has resided with, and been embodied in, the organisms themselves” (Butler 1879, p. 24–33).

  26. 26.

    My problem exists because some excellent Darwinists even believe that evolution can be fully explained by only two things: (1) The variability of the genome whose variations are obviously a matter of chance are completely independent of the organisms’ activities and preferences; and (2) The physical environment, where ‘physical’ may include, of course, the physical presence of other organisms” (Popper 1986, in Niemann 2014, p. 119).

  27. 27.

    Darwin, as you all know, believed in sexual selection. And he believed that sexual selection was a kind of natural selection. But this is only if we take the niche of the male, to which the female belongs, as the niche that is here important. It can be easily show, all of you can think of this when you go home, that if we take a niche that covers both male and female, then sexual selection is a refutation of natural selection. So it depends on the concept of niches whether sexual selection fits into the scheme of natural selection or refutes it. If you take the niche of the male, then the female is part of the niche and the male must please the female by such things as tail or horns, or I do not know what, which may not be very useful for natural selection. But if you take the niche for male and female together, then most of the examples of sexual selection are a worsening of adjustment, of the adaptation, to this common niche. They are an improvement of adaptation to the niche of the male and a worsening of adaptation to the common niche of male and female” (Popper 1986, in Niemann 2014, p. 127–128).

  28. 28.

    One of my assertions is that the preference for better niches is the main thing that leads to Darwinian evolution. The organisms are active. They search a better niche. And then this niche, this environment, ensures somehow that the better adapted organisms leave more offspring. And in this manner we get specialisation and more adaptation” (Popper 1986, in Niemann 2014, p. 122).

  29. 29.

    I do not defend Lamarckism as it is today called, that is to say, the inheritance of acquired properties” (Popper 1986, in Niemann 2014, p. 127–128).

  30. 30.

    I assert that every animal is born with expectations or anticipations, which could be framed as hypotheses; a kind of hypothetical knowledge. And I assert that we have, in this sense, some degree of inborn knowledge from which we may begin, even though it may be quite unreliable. This inborn knowledge, these inborn expectations, will, if disappointed create our first problems; and the ensuing growth of our knowledge may therefore be described as consisting throughout of corrections and modifications of previous knowledge” (Popper 1972, p. 258–259).

  31. 31.

    It seems to me of considerable importance that we are not born as selves, but that we have to learn that we are selves; in fact we have to learn to be selves. … [by] developing theories about ourselves” (Popper and Eccles 1977, p. 109).

  32. 32.

    “The believer—whether animal or man—perishes with his false beliefs.” (Popper 1972, p. 122)

  33. 33.

    I do not claim that I have refuted materialism. But I think that I have shown that materialism has no right to claim that it can be supported by rational argument—argument that is rational by logical principles. Materialism may be true, but it is incompatible with rationalism, with the acceptance of the standards of critical arguments; for these standards appear from the materialist point of view as an illusion, or at least as an ideology” (Popper and Eccles 1977, p. 81).

  34. 34.

    “Indeterminism—or more precisely, physical indeterminismis merely the doctrine that not all events in the physical world are predetermined with absolute precision, in all their infinitesimal details” (Popper 1972, p. 220).

  35. 35.

    We have to assume, difficult as this may be, that it [consciousness] is a product of evolution, of natural selection. Although this might constitute a programme for a reduction, it is not itself a reduction, and the situation for the reductionist looks somewhat desperate; which explains why reductionists have either adopted the hypothesis of panpsychism or why, more recently, they have denied the existence of consciousness (the consciousness say, of toothache) altogether. Though this behaviourist philosophy is quite fashionable at present, a theory of the nonexistence of consciousness cannot be taken any more seriously, I suggest, than a theory of the nonexistence of matter. Both theories ‘solve’ the problem of the relationship between body and mind. The solution is in both cases a radical simplification: it is the denial either of body or of mind” (Popper 1974, p. 272–273).

  36. 36.

    Compton describes here [in a preceding quote] what I shall call ‘the nightmare of the physical determinist’. A deterministic physical clockwork mechanism is, above all, completely self-contained: in the perfect deterministic physical world there is simply no room for any outside intervention. Everything that happens in such a world is physically predetermined, including all our movements and therefore all our actions. Thus all our thoughts, feelings, and efforts can have no practical influence upon what happens in the physical world: they are, if not mere illusions, at best superfluous byproducts (‘epiphenomena’) of physical events” (Popper 1972, p. 217).

  37. 37.

    To push this point further, in the Medawar Lecture, I think it is revealing that Popper spends his term advocating ‘active’ Darwinism in the discussion of animals only—and I would read him more specifically as talking about vertebrates because only they have a kind of generalised learning because of their centralised nervous system (in a way that makes individual capable of expressing its own unique personality). Further, Popper gives little consideration of the animals, plants and micro-organisms that form sedentary (or sessile) individuals that do not have much control over their environment. I do not mean to imply that they cannot engage in ‘niche construction’, but sedentary species clearly must have a restricted ability to do so in comparison to motile species. The fact that there are degrees to which Popper’s ‘active Darwinism’ might be better for understanding some species over others is very different from disputing the ‘general case’, as Popper does. Additionally, Popper gives no discussion of selfish genetic elements, intragenomic conflict and horizontal gene transfer and other phenomena of living things that undermine the importance of individuals as coherent/unified learning agents. From an empiricist perspective, I think that Popper falls into a rationalist trap, which was eloquently stated by Hume: “What peculiar privilege has this little agitation of the brain which we call thought, that we must thus make it the model of the whole universe?” (Hume 1779, p. 134). In this reading, Popper applies the structure of his own way of thinking to the objective world as if the objective world had the same structure; hence why Popper thought it was legitimate to draw parallels between the growth of scientific knowledge and evolution by natural selection. In other words, I think that Popper over-states the degree to which organisms choose their environment because his philosophy lends him toward being anthropocentric.

  38. 38.

    The critical feature of selection is sometimes misconstrued (as Noble does so), and so I will clarify. Although the paradigmatic selection process would be random variation, a bias in the process of mutation does not matter in as far as the bias does not influence the outcome of the selective process—which is to do with a feature of the environment that does the selecting. This is why the word ‘blind’ is often preferred to ‘random’.

  39. 39.

    As an aside, I think it would be possible to make the reverse argument that instruction underlies selection, but to do so would require the physical laws of the universe to be construed as ‘instructions’. In this implicitly causally deterministic framework, natural selection would proceed from the physical laws of the universe because the physical laws permit selection to operate. This argument is not totally vacuous, hence why natural selection can be simulated in a computer that operates by a series of instructions. However, I would argue that this argument alienates an important aspect of natural selection, which is the medium of the replicator. The mechanics of genome replication has a huge impact on the direction of the evolutionary change resulting from selection—and the degree to which different kinds of traits can be more or less adaptive, so I am not sure how useful this perspective is. Further, given its causal determinacy, I am not sure how much is reinforces the active problem-solving perspective of organisms.

  40. 40.

    It is common to think of constraints in a negative fashion – as preventing things from happening, and thereby reducing the variety found in nature. But if the process of producing variation is open-ended, the introduction of constraints can channel the variation, and by directing it, produce much further or deeper exploration in a given direction than would otherwise be possible. Constraints can thus play a creative and, in one sense, ultimately progressive role. This is a deep truth, not only about evolution, but about problem-solving and exploration in general. It is why Darwin was right in 1859 when he saw natural selection as a creative force, and why his critics who saw selection only as playing a negative role by eliminating variety were wrong” (Wimsatt and Schank 1988, in Nitecki 1988, p. 235).

  41. 41.

    No scientist is admired for failing in the attempt to solve problems that lie beyond his competence. The most he can hope for is the kindly contempt earned by the Utopian politician. If politics is the art of the possible, research is surely the art of the soluble. Both are immensely practically-minded affairs” (Medawar 1967, p. 97).

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Madgwick, P. (2021). Agency in Evolutionary Biology. In: Parusniková, Z., Merritt, D. (eds) Karl Popper's Science and Philosophy. Springer, Cham. https://doi.org/10.1007/978-3-030-67036-8_12

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