Agency in Evolutionary Biology

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.

1 Why Does Evolutionary Biology Give a Privileged Role for DNA?

Contemporary evolutionary biology is a vast and loosely-connected discipline, so it is very hard to give an all-encompassing account of what it is all ‘for’, but I am nevertheless going to try. The vast majority of evolutionary biologists are working within a tradition that stems from Charles Darwin’s (1859) The Origin of Species (hence the label ‘Darwinism’).¹ However, the contemporary tradition of evolutionary biology has been arrived at after a great discontinuity, which has been described as ‘the eclipse of Darwinism’.² In this way, the contemporary tradition is often considered to have its foundations laid after the discontinuity in the research tradition stemming from Julian Huxley’s (1942) The Modern Synthesis. To many critics of contemporary evolutionary biology—not least those like Noble (2006, 2016) concerned with the privileged role of DNA in evolutionary theory, the ‘Neo-Darwinism’ in The Modern Synthesis was where it all went wrong. I am going to address what happened at this critical juncture circuitously, by following the chain of reasoning from the statement of a problem that evolutionary theory sets out to explain and to the capitulation of ‘the privileged role of DNA’ on the way to its resolution.

1.1 What Is Evolutionary Biology All About?

Although Darwin’s The Origin of Species represents the intellectual birth of mainstream evolutionary biology, the question at the heart of this book was a much older one: the problem of adaptation.³ Yet, the way of approaching the problem was comparatively contemporary. Following in the tradition of British empiricism,⁴ Darwin sought to explain adaptations with reference to features that were ‘external’ to the organism. The choice of this approach was heavily influenced by William Paley, who was by no means the originator of this externalism, but was amongst its most effective and influential advocates. Paley contended that the reason why the forms and behaviours we see in nature are one way rather than another has nothing to do with the individuals in question.⁵ Instead, Paley argued, the forms and behaviours must be explained by the existence of a Creator. Darwin naturalised Paley’s teleological argument and repurposed it to support his theory of adaptation through evolution by natural selection, which is famously based on a great analogy to animal and plant breeding.⁶ The Origin of Species is, for the most part—and almost to the point of tediousness, a great catalogue of evidence collected from ‘the many treatise devoted to this subject’ of selection by breeders. But, in all important senses, Darwin left unchanged the externalist style of reasoning that was championed by Paley wherein individuals have adaptations because of some feature external to those individuals. Such externalism was in great contrast to the thrust of pre-Darwinian evolutionary theory, especially stemming from Lamarck (and continental rationalism).⁷ So, what is the aim of evolutionary biology? In sweeping terms: to explain adaptation. But, to the extent that a research tradition is both a problem and a way of approaching that problem,⁸ the problem of evolutionary biology is also set within an externalist method of enquiry.

As I have eluded to already, Darwin did not instigate a successful research tradition within his own lifetime—though he was nonetheless well-respected.⁹ Instead, there were many apparently insurmountable criticisms, though it is interesting that the constructed history of this time by evolutionary biologists tends to focus on one: “The biggest blank on the evolutionary map, however, concerned variation and its inheritance. The theory of mutation on a mendelian basis is the first adequate attempt to fill the gap” (Huxley 1942, p. 109). Or, as was remarked after The Modern Synthesis (from which the quote above is taken) was published: “The question Darwin failed to answer was actually a simple one. Survival of the fittest what?” (Alexander 1979, p. 23). Progress toward an answer to this question started with the studies of the mechanism of inheritance by Gregor Mendel, which led to the development of population genetics. For those involved in this new field, the world of individual organisms rapidly becomes reconceptualised in terms of a genetic accounting.¹⁰ Underlying this shift in focus from individuals to genes, there was also a drastic reconceptualization of the very phenomena at the heart of scientific enquiry: “evolution is a change in the genetic composition of populations” (Dobzhansky 1937, p. 11).

In this way, The Modern Synthesis is actually a rather curious text: on the one hand it was revolutionary, but on the other it was also incredibly dated. For example, Huxley explains natural selection in the form that Darwin presented in The Origin of Species—i.e. in the form that was not watertight and hence experienced an ‘eclipse’. Huxley thought that population genetics vindicated Darwin’s argument, when instead it radically transformed it. For this reason, Peter Medawar is reported to have remarked after Huxley delivered a talk: “The trouble with Julian [Huxley] is that he really doesn’t understand evolution” (Dawkins 2013, p. 269). For this reason, the constructed history of this time by mainstream evolutionary biologists gives much more attention to a later work by George Williams (1966), called Adaptation and Natural Selection.¹¹ This book was enormously influential in firmly placing the externalist approach to adaptation from Paley, which is so prominent in Darwin’s description of evolution by natural selection, in centre-stage.¹²

Williams brings a new philosophical rigour to the concept of adaptation, only licensing its use under restrictive circumstances: describing a trait as an adaptation is a specific hypothesis about what trait is being considered, what functions that trait serves and what aspect of the environment drives the trait’s selection.¹³ Central to this reinstatement of Darwin’s question of adaptation was an abandonment the individual-centric description of evolution by natural selection on traits and a rehousing of the basic idea within a gene-centric framework.¹⁴ This may seem a little confusing, because Williams is also looked back to for asserting individual selection over group selection, but this assertion is made because Williams is thinking about those entities as genetically-accounted.¹⁰ This line of reasoning was taken to its logical extreme by Richard Dawkins (1976) in The Selfish Gene, who extolled Williams’ gene-centric approach to evolution with great flare.¹⁵ Within Dawkins’ ‘seductive’ description, there is a definite hardening of what evolutionary biology is all about. When individuals are viewed as ‘throwaway survival machines’, attention necessarily refocuses on what is more permanent—the genes. But, one might think, surely there are other entities that could have enough permanence to also be an important part of evolutionary change? Dawkins gives a thorough exhibition of this point to discuss why genes take centre-stage: “What, after all, is so special about genes? The answer is that they are replicators” (Dawkins 1976, p. 191). Thus, whilst biologists might say ‘genes’, it is really replicators that are at the heart of evolutionary explanations. As Dawkins described, replicators have a degree of permanence unlike any other biological entities because they have the stability, fecundity and fidelity (of replication) to survive on evolutionary timescales. Whilst Dawkins does flirt with the idea of a second replicator within human culture (coining the term ‘meme’), he does not think that biological evolution is impacted by any replicator other than genes¹⁶—and mainstream thought still concurs with this opinion.¹⁷ The hard-won replicator perspective on evolution is widely celebrated because it makes us think clearly about ‘what’ is being selected.¹⁸

So, what is evolutionary biology all about? In the broadest sense, it is about how living things change over the generations. But, for the most part, this line of enquiry is about the genetics of adaptation: why we see one trait rather than another, from the externalist perspective of the features of the environment that lead to the selection of some genetic variants rather than others.

1.2 What Is Evolutionary Biology’s Concept of Agency?

I have set evolutionary biology firmly on the philosophical foundations of British empiricism. In this light, unsurprisingly, evolutionary biology’s concept of agency is very much in-keeping with this tradition¹⁹ in viewing agency as a metaphor—not a ‘fact of nature’. Consequently, there is no problem in talking about genes, individuals or groups as agents, but there is a need to be disciplined. Agency is a useful way of talking about entities that take decisions, so can in principle be applied to many biological entities. But, as Williams (1966) argues in Adaptation and Natural Selection, we should not confuse scenarios where a single or multiple agencies are at work because the outcome can be very different (which was the cause of Wynne-Edwards’ group selection controversy).

Evolutionary biologists tend to use this concept of agency in very loose ways. For example, although I have stated that agency can be a useful way of talking about genes, individuals or groups, in each case most evolutionary biologists discuss individuals and groups as genetically-accounted (i.e. as collections of genes). Because natural selection acts on phenotypes and acts by changing genotypes, evolutionary explanations often focus on a genotypic change but explain it via the phenotypic consequences of competing genotypes. The blurring of this replicator-vehicle distinction is something of a bad habit, but it can make arguments much easier to follow by observing the convention that the ‘individual’ refers to whatever genotypes of that individual are currently relevant. I would also add, here, that there is now a thriving research tradition stemming from Leo Buss’s (1987) The Evolution of Individuality where the coherence of biological entities as discrete individuals is understood as a derived trait along a continuum of individuation at different phenotypic (or vehicular) levels across the diversity of current lifeforms (see also Maynard Smith and Szathmáry (1995) The Major Transitions in Evolution).

One may wonder, how does this concept of agency gel with common-sense notions like free will? When The Selfish Gene was published, I think that the philosophical impact of the idea that your genes may have contrary interests to your own presented the ‘self’ as something of that old Cartesian duality in suggesting a ‘ghost in the survival machine’. This is not what evolutionary biology implies. Instead, following empiricism, the general view is one of compatibilism between causal determinism and human freedom²⁰: all events are seen as part of chains of cause and effect, irrespective of whether or not those causes or effects are necessarily observable, and human freedom is viewed as a subjective statement about our incomprehension of how our own causal mechanisms work (rather than inviting speculation on whether or not there are unaccounted supernatural sources of causation).

1.3 Why Does Evolutionary Biology Give a Privileged Role for DNA?

I have stated, in broad terms, that evolutionary biology is about how living things change over generations, and this means understanding why we see one trait rather than another, from the externalist perspective of features of the environment that lead to the selection of some genetic variants rather than others. So, when thinking about the claim that evolutionary biology gives a privileged role to DNA, there are two basic responses here. The first is to deny that evolutionary biology does give a privileged role to DNA in its explanations of how traits change. I think it would be possible to argue that this misunderstands the way in which genetic explanations of adaptation draw links between the environment and DNA, as a hypothesis that connects some external feature of the environment with some internal feature of individuals. The second is to accept that there is a kind of privilege at work, which is afforded to replicators. As the only widely-accepted replicator is the gene (i.e. DNA), mainstream evolutionary biology is principally about the genetics of adaptation. Most evolutionary biologists would launch into the first response, but what would follow would be a rather dull, long-winded case-by-case exposition of paradigmatic examples of how evolutionary biology asks a question and finds its answer in a genetic difference. But I am not really sure that gives a serious treatment of the criticism, which I think is less about paradigmatic examples and more about the way in which the genetic focus of research can by assumption exclude alternative (and interesting) sources of explanation from the enquiry. In this way, I am going to only address this second response.

Claims of replicators that are built of other materials than DNA are controversial, but they are ‘in the air’ at the moment with the rise of epigenetics. These are not woolly suggestions of ‘memes’ or suchlike, which have dropped out of favour because it is not clear that the study of ‘cultural variants’ really gains very much from the analogy to genes (because the mechanism of genetic replication is nothing like how organisms learn).¹⁵ This is actually a critical point: the ‘eclipse of Darwinism’ was made possible by the fact that Darwin’s argument in the absence of a mechanism of inheritance was not guaranteed to be correct. For a non-DNA replicator, the mechanism of inheritance would have to be known for it to be more than an interesting speculation—and perhaps some epigenetic systems are sufficiently well-characterised to be worthy of exploration.

What would need to be demonstrated to evidence a non-DNA replicator? I don’t view this as a systematic answer, but there would (at least) need to be a clear demonstration that the candidate biochemical was capable of traits that are independent from variation in the DNA-replicator. Consequently, instances where a candidate biochemical is inherited but not replicated would be insufficient. These might include, for example, regulatory biochemicals that are given by a mother to her unborn infant during pregnancy to ‘prime’ that individual for the environment they are about the experience. Even if these molecules were inherited across multiple generations, they would only survive on evolutionary timescales if they were being replicated. Regeneration of a regulator does not count as replication, because it is still under the control of the DNA-replicator. That is not to say that I, as an evolutionary biologist, do not find this fascinating, but I would tend to view priming as interesting from a different perspective. The question that interests me is about the selection on the genetic variant that enables priming rather than whether or not individuals have a primed phenotype. To date, and to my knowledge, there are not epigenetic molecules that are anything more than inherited-regulatory molecules that act as primers.²¹

For those interested in epigenetic replicators, I think there is one consideration that is always worth bearing in mind. Even if a non-DNA replicator were discovered, which I would keep an open mind toward: how would evolutionary biology change were a non-DNA replicator discovered? I would suggest, not very much. The vast majority of genetic explanations of adaptation would still hold, because the vast majority rest on the experimental manipulation of individuals with different genetic variants in order to confirm what feature of the environment selects a particular genetic variant (and its associated traits). Given this, genetic change must be the predominant explanation of how living things evolve. However, a non-DNA replicator would introduce a new dimension for evolutionary biology. Just as the quirks of the genetic mechanism influence how traits evolve, quirks of the new replicator’s mechanism would presumably do likewise. And, I would suppose, there would also be room for conflict between types of replicator. In the history of life on earth, it is generally thought that there have been other types of replicator and that the genetic code (built on DNA) has selectively out-competed other systems because it is a good medium of replication.²² But, it is not widely held that other types of replicator beyond those built from nucleic acids are important for the 3.8 billion years of life on earth that we currently know about. And, of course, if there were convincing evidence to contrary, opinions would change.

So, why does evolutionary biology give a privileged role to DNA? Given that evolutionary biology is trying to explain why traits change over time in one way rather than another, evolutionary biology privileges DNA in its explanations because the only genes (i.e. DNA-replicators) can persist on the relevant evolutionary timescales.

2 Why Is Popper’s ‘Active Darwinism’ Problematic?

I have presented an explanation of why evolutionary biology is set up the way it is, and now I want to turn to the alternative concept that was advocated by Popper and pushed for with renewed vision by Noble.

2.1 What Is Popper’s Reading of Evolutionary Biology?

Popper’s earliest evolutionary ideas were first expressed in The Poverty of Historicism (1957) and came to the fore in The Logic of Scientific Discovery (1959) where the growth of knowledge was described as a process of cumulative error elimination. But Popper did not see an immediate parallel with his theory of scientific progress and evolutionary biology. By the time of his Intellectual Autobiography (1974), Popper started to make these connections but was rather wary of ‘Darwinism’: “I have come to the conclusion that Darwinism is not a testable scientific theory, but a metaphysical research programme—a possible framework for testable scientific theories” (p. 134). For him, this rests of the premise that: “Darwinism does not really predict the evolution of variety. It therefore cannot really explain it. At best, it can predict the evolution of variety under “favourable conditions”. But it is hardly possible to describe in general terms what favourable conditions are—except that, in their presence, a variety of forms will emerge” (p. 136). It is nonetheless clear that evolutionary biology is especially problematic for his understanding of scientific progress, but he firmly states: “And yet, the theory is invaluable” (p. 137). In this early interaction, I think we can see how Popper is seeking to isolate a specific strand of evolutionary biology as ‘Darwinism’, as opposed to a more general evolutionary approach which he sees himself as a contributor toward.

Following on from ideas developed in the Spencer Lecture (1961) entitled Evolution and the tree of knowledge—which was the basis of a chapter in Objective Knowledge (1972), Popper controversially expresses dissatisfaction that evolutionary biology can adequately explain cumulative adaptation, following the suggestions of others that there must be ‘orthogenetic trends’ to funnel variation in specific directions. But at the time of completing Objective Knowledge (1972), unambiguously stated that the “Neo-Darwinist theory of evolution is assumed” (p. 242), and he went on to elucidate twelve theses on which evolutionary theory rests, which can be broadly summarised en-masse as applying his thinking of cumulative error elimination within scientific progress to nature. I would suggest that he was starting to see his ideas on the growth of knowledge within the broader context of evolutionary thought (i.e. seeing epistemology as an evolutionary science), alongside a long-standing unease with something in the contemporary science. Popper’s insistence that there is a common mechanism at work within scientific progress in knowledge and adaptive evolution in nature²³ was in tune with the zeitgeist, where there was enthusiasm for ‘Universal Darwinism’²⁴ and the broader development of ‘evolutionary’ subdisciplines (most notably) in economics, computer science and psychology.

Although it is not clear at exactly what stage Popper read various works of Samuel Butler, especially Evolution: Old and New (1879) where the basic distinction between ‘active’ and ‘passive’ Darwinism is first made,²⁵ Popper acknowledges a debt toward him in his Intellectual Autobiography (1974) whilst expressing a general disdain for other ‘evolutionary philosophers’. Many of the concepts of Popper’s Medawar Lecture (1986, published in Niemann 2014) are within Butler’s Evolution: Old and New, but I suspect that Popper arrived at Butler’s perspective semi-independently in marrying together a dissatisfaction with a specific strand of evolutionary thought and the comparisons with (and generalisation of) his ideas on the growth of the scientific knowledge.

Within the Medawar Lecture, Popper clearly expressed an understanding of the essential aim of what evolutionary biology was about,²⁶ but disagreed with much of the language in which ideas are presented. This disagreement led him to discuss natural and sexual selection as competing theories,²⁷ when most evolutionary biologists would the latter as a subcategory of the former. Popper viewed the role of organisms’ preferences for choosing their own niche to be broadly ignored with contemporary evolutionary theory,²⁸ and consequently asserted a much greater role for problem-solving (i.e. learning) in the general picture of how organisms are selected. Nevertheless, I think is important to remember is that Popper was contrasting two forms of Darwinism, in that he wasn’t suggesting that Darwin’s research tradition was ‘wrong’—or advocating some alternative like Lamarckism.²⁹ Instead, I think his aims in the Medawar Lecture were more in the vein of stating some things that appeared odd within the framework of contemporary evolutionary theory from the opinion of an outsider. And, in short, what struck him as odd was evolutionary biology’s concept of agency.

2.2 What Is Popper’s Concept of Agency?

Popper defends a common-sense notion of agency, which he exclusively attributes to organisms, based on the fact that you have free will in the very literal sense that you have real choice that is not determined by any prior events (contra causal determinism)—but it is fair to say that his views here are quite hard to discern. Prior to the Medawar Lecture, Popper takes the view that human agency is somewhat exceptional in contrast to other animals’ agency—though we share some basic features.³⁰ But, whilst human knowledge is primarily learnt about their world and consequently agency develop as an ability to make choices,³¹ animal knowledge is primarily genetic—having been acquired through natural selection.³² Popper clearly had an uneasy relationship with what he referred to as either ‘materialism’³³ or ‘determinism’³⁴—but what I will refer to as (British) empiricism. My reading is that Popper struggled to work out what kind of a claim he was wanting to make: was free will a claim about our imperfect understanding of human behaviour or a claim about how humans are? Here, Popper sided with rationalism rather than empiricism, to assert that consciousness (and hence free will) is an undeniable objective fact.³⁵ To a rationalist, consciousness is the first and most undeniably true fact of existence because it does not rest on anything other than introspection. But, following Searle’s (1999) terminology, Popper seems to conflate statements that are epistemically objective (i.e. claims about what is from my perspective) with statements that are ontologically objective (i.e. claims about what is). The former are dependent on current evidence, but the latter are not. In contrast with the empiricist tradition, free will is an epistemically objective ‘illusion’¹⁹—but that is not to say that behavioural science would ever have enough knowledge to predict human behaviour with any reasonable accuracy. I have often wondered whether Popper’s view was influenced by his point in history, where he had seen the damage that could be done by entertaining a nihilistic view of the objective world.³⁶ I might also add that I have always been baffled why indeterminism might somehow make room for free will in the objective world (what Popper called World 1), when its behaviours remain statistically definite.

2.3 Why Is Popper’s ‘Active Darwinism’ Problematic?

I do not think there is any other way to construe my reading of Popper’s division of ‘active’ and ‘passive’ Darwinism: it is a false dichotomy. The thing that really makes me firm about this conclusion is Popper’s treatment of sexual selection, which he argues contradicts natural selection.²³ I understand what he means, namely that what makes an individual adapted to survival can differ from what makes an individual adapted for reproduction—which is not a controversial statement. But natural selection is generally used as the overarching idea of any type of selection, of which sexual selection, kin selection, fecundity selection, mortality selection etc. are subtypes. More to the point, I see no deficit in the current research paradigm stemming from Darwin, who gave us both the concepts of natural and sexual selection. I reject Popper’s assessment of theory only treating the male’s choice (or niche), which probably stems from Popper being unaware of traits that are associated with female choice—but nevertheless if he was aware of these cases then he glossed over them as he was running out of time at the end of the lecture. In this way, much of this disagreement about sexual and natural selection must surely reflect a problem of language, as Popper was clearly using terms in a different way than evolutionary biologists' do. I wonder how much of the general idea of ‘active Darwinism’ is of the same flavour, but I am not going to focus on this exposition because it seems rather dull.

At a deeper level, the problem with ‘active Darwinism’—in as far as there is one that extends beyond a rephrasing of the ideas in ‘passive Darwinism’—relates to Popper’s discussion of how organism’s choices impact how they evolve. I do not think that there is any disagreement that, say, the sexual preferences of organisms can be important in determining how evolution proceeds. I think there is room to doubt two things: first is the generality with which this applies, and second is the essentiality to a general explanation of natural selection.

Popper is right to assert that many organisms have preferences that change how they interact with the environment, and consequently how selection acts on them; but when Popper encounters this, he asks “How do those preferences impact evolution?” when an evolutionary biologist would ask “Why are those preferences adaptive?”. If those preferences were arrived at randomly, they would be of little interest to me as an evolutionary biologist because they would not be adaptive. Preferences are only going to be adaptations if they have the ability to be passed on in the longer-term (i.e. over many generations), which would need them to be produced by replicators. So, the fact that preferences change evolution is point of agreement, but Popper has inverted the causality to suggest the preference evolves before the gene that enables an individual to express that preference. Popper gives little indication about where this preference might come from beyond ‘active problem-solving’, which both Popper and his commentators have likened to a Baldwin effect, where learnt preferences (i.e. non-genetic adaptations) impact genetic evolution. As Popper seems to be aware, there is nothing incompatible between the Baldwin effect and what he calls ‘passive Darwinism’—and the Baldwin effect is even incorporated into Huxley’s The Modern Synthesis. The difference is more that Popper assumes that the Baldwin effect is the ‘general case’ and other cases are the exception (hence favouring the phrasing of his active Darwinism), whilst evolutionary biologists assume the opposite. In defence of the position of most evolutionary biologists, I could now launch into a set of evidence that not many organisms (if not only one) are capable of generalised learning in such a way that their learnt preferences meaningfully impact their genetic evolution in order to show that most lifeforms evolve in a much more ‘passive’ way that Popper supposed.³⁷ But, for me, the crux is really settled by my second point.

Organisms do not need to be active problem-solvers for them to evolve by natural selection, and so problem-solving does not really explain adaptation in general terms. It may well be true that generalised learning has a much greater role in evolution than most evolutionary biologists tend to think, but natural selection would work on entities that are incapable of learning. Indeed, evolutionary biologists tend to mostly work with genes, which may react to different environments in different ways (which we can understand as a probabilistic ‘reaction norm') but are fundamentally inert chemicals that do not change their own base composition. Instead, environmental factors may cause them to mutate as they are passed down the generations, and therefore any adaptations that they contribute toward are only the result of natural selection. On this point, it can be useful to follow evolutionary epistemology’s portioning of an adaptation into components of instruction and selection (Plotkin 1994). The basic idea here is that adaptation can come about through two basic sources: instruction refers to following some ‘rules’, and selection refers to environmental feedback on blindly-generated variation.³⁸ Classically, these two sources of adaptation can be thought of as extremes on a continuum between rules uniquely specifying a single adaptive variant and the generation of multiple variants that are then whittled down to a single adaptive variant. A preference is an instruction, but the question is how any adaptive properties were arrived at. If the preference is innate, then it was arrived at through selection on genotypic variants. If the preference is learnt, then it was arrived at through instruction by some phenotypic set of rules. The continuum perspective masks that those phenotypic rules are only going to successfully lead to adaptation if they are the result of a selective process (i.e. by selection on genotypic variants that specify learning rules). Therefore no matter how you look at it, in the ultimate sense, adaptation is arrived at through natural selection somewhere in the system, but it doesn’t necessarily have to be natural selection in a straight-forward manner. I would also say, tying this back to biology, adaptation is arrived at because of the natural selection of genotypic variants that underlie behaviour, or the learning rules that govern behaviour. In this way, it is natural selection not problem-solving (i.e. learning) that is essential to adaptation.³⁹

Perhaps one could argue that this restricts the scope of evolutionary biology’s explanation of adaptation, but I think it clarifies something very important. If there is any adaptation as a result of learning, that adaptation is either the result of the natural selection of genes governing how behaviour changes in response to some feature of the environment or the result of a secondary phenotypic process of selection that is enabled (but not directed) by genes. The second case, we might consider as ‘open-ended’ or ‘generalised’ learning, though of course how open-ended it is depends on the system’s constraints (just as modern genes are constrained by protein biochemistry). To explain a trait as an adaptation would require an intimate knowledge of the way selection works in that system (just as natural selection only made sense given genetics). In the context of genes, this is often described as suggesting that genetic ‘constraints’ are an important part of adaptive explanation because of their creative role in how selection works.⁴⁰ What little we do know about learning systems is that they vary across the diversity of life, and so the constraints in these systems are never going to be universally shared (unlike for the genetic code, which is pretty much universal). The point I want to make here is this: even if evolutionary biologists were interested in learnt adaptations, we would explain them with the same externalist mindset as we apply to genetic adaptations. In this way, we would still direct focus toward how features of the external environment cause features of the internal structure that we see, rather than really treating individuals as active problem-solvers.

3 What Was Popper’s Criticism Really About?

This brings me on to my final set of thoughts. I find it hard to believe that Popper cannot have considered most of the arguments that I have just raised both for evolutionary biology’s framework and against his suggested alternative. The question is, why did he continued anyway? I don’t think that he was really trying to revolutionise evolutionary biology by unveiling some fatal flaw in contemporary research. Instead, I think he was trying to push the analogy of evolutionary change as a learning process in order to expose something odd about the way evolutionary biology conceptualises agency. I think Popper rightly sensed the externalist tendency of evolutionary biology to explain adaptations with appeal to features of the environment, though I do not think that he recognised this externalism explicitly. Given that Popper is the champion of common-sense, I think Popper’s discomfort with evolutionary biology came from his unease with the way that it flaunts agency as a metaphor—which stands very much in contradiction of his rationalist account of science as yielding objective knowledge about reality. I think that many people would instinctively sympathise with Popper’s position, especially for those in contemporary thought that look to evolutionary biology as orchestrating a modern (and atheistic) Creation Myth, whereupon I think it is natural for many people to feel like there should be some greater prominence of the individual within this scientific epic. The way in which evolutionary biology asserts the insignificance of agency is omnipresent in the way in which, even when organisms are discussed, organisms tend to be talked of in terms of their genetic accounting only.

Prior to the Medawar Lecture, I have suggested that there was a tension in Popper’s thoughts on evolutionary biology—hence why he both lavished it with praise and yet gave it special treatment as an inconvenient anomaly. By the time of the Medawar Lecture, I think that Popper had resolved some of this tension by asserting that agency objectively exists and is an important part of the causal structure of the objective world, rather than asserting that agency has a subjective existence as a metaphorical way of thinking about the objective world. However, I do not think that Popper critically assessed why this disagreement about agency came about. I have characterised this as Popper’s favouring of rationalism over empiricism in asserting the existence of agency prior to any evidence which may suggest an alternative conclusion. Within rationalism, agency is the bedrock of all human understanding which is built from ontologically objective knowledge; within empiricism, agency is more often used as a metaphor (or ‘thinking tool’), and human understanding is built from epistemically objective knowledge (which may or may not turn out to ontologically objective). In this regard, Popper’s own philosophy of ‘critical rationalism’ is—to some extent—bridging the divide, but in other ways it is also a bridge built from one side on a rationalist foundation. Along with other scientists, evolutionary biologists tend to admire Popper as ‘their’ philosopher of science, in defending a common-sense world-view held by most scientists. But, in the details, I think that many scientists would defend the same world-view but from an empiricist foundation (perhaps, ‘critical empiricism’?).

In this way, I think it is inaccurate for Noble and others to use Popper as someone who was ‘on their side’ against the views expressed in The Modern Synthesis because I think that Popper’s complaint with evolutionary biology was a philosophical one relating to agency. Popper thought very favourably of Medawar’s critique of Teilhard de Chardin’s evolutionary theology, wherein scientific research was described as the ‘art of the soluble’.⁴¹ Perhaps influenced by the empiricist foundations of evolutionary biology, Medawar was expressing the fact that a good research scientist spends their time solving problems rather than building syntheses. Particularly in biology, a synthesis is always going to be constructed as a teaching aid for general intuition rather than as a rigorous statement of universal truth because there will always be an exception. To my mind, focusing criticism on The Modern Synthesis as a seminal work is a fascinating construction of the history of evolutionary theory because, as I and others have argued, it actually had very little impact compared to other contemporary works. Further, the word ‘synthesis’ makes it a wonderful straw-man; ecology does not have a ‘modern synthesis’ equivalent but is instead a looser collection of canonical concepts and so it is much harder to decry its failures in this way.

4 Conclusion

So, where does this leave us? Popper’s foray into evolutionary biology is fascinating because it represents a collision of world-views. I am not sure that Popper gets everything right, and I am not sure that Noble is correct that we need to rehabilitate Popper’s views of evolutionary biology—nor do I think we will ever agree on that one. But I respect that there is something non-trivial about these disagreements, which deserves further discussion. I think much of the disagreement comes from the competing treatments of agency within rationalist and empiricist traditions, and so I think that the non-trivial elements of the disagreement are philosophical in nature, rather than relating to anything that could be changed on the practical side of the established facts that either tradition could use to support their position. Perhaps by simply recognising the nature of this disagreement, a lot of misrepresented ‘hot air’ can be avoided.