Introduction and interview: Ramón del Buey

Published in Spanish in the journal: Papeles nº158

It is symptomatic that the French philosopher Bruno Latour entitled his lecture accepting the latest Kyoto Prize: “How to react to a change in cosmology”. What would our reaction have been if we had experienced the Copernican revolution first hand? And if we would be facing now a similar revolution in Biology?

The interview below is an opportunity to transfer such a thought experiment to a more real-life questioning situation. On April 6, 2022, the prestigious journal Paleobiology, edited by Cambridge University Press, published “Applying the Prigogine view of dissipative systems to the major transitions in evolution“, a research on the evolution of the complexity of life that is destined to occupy an important place not only in the history of science, but also in the thoughts (and actions?) of any soul concerned with understanding our place in the cosmos.

The article was written by Carlos de Castro (Department of Applied Physics, University of Valladolid) and Daniel W. McShea (Department of Biology, Duke University), based on a question as simple as it is transcendental: why does the trajectory of the degree of complexity of organic systems, which accelerates exponentially over time according to empirical observations, not coincide with the predictions of neo-Darwinism, an explanatory model for which a slowdown in evolution is to be expected? The answer offered by the authors consists in defending a specific type of feedback between the upper and lower levels of these organic systems, based on the thesis that the causal chains that occur in this feedback would not follow a solely ascending orientation, in such a way that we could explain everything as interactions of subatomic particles, but, on the contrary, the causality would also be descending, in such a way that the totalities, especially the most encompassing organic ones, would causally explain the reality of the functions and interactions of matter and energy that we finally find in the relations of the entities or beings that conform with their interaction these organic totalities. The article, as its title indicates, applies a tool from thermodynamic physics, Prigogine’s trinomial, to a field studied by Biology, the history of evolution and, specifically, the history of what are known as Major Transitions in Evolution (hereinafter MTE), that is, the most important changes in the complexity of organ systems, such as the transition from prokaryotic to eukaryotic cells, or the transition from eukaryotic cells to multicellular organisms. If you are not familiar with Prigogine’s ideas or the Gaia theory, three additional texts are provided at the end of the interview to facilitate understanding. But it is also possible that the astonishment that follows the reading may be of a different kind: will it be our reaction to a new change in cosmology?

1. How did a biologist and a physicist collaborate for such a transdisciplinary research?

Carlos: The thermodynamics advocated by Ilya Prigogine is one of the two “physical” pillars on which I rely to explain how an organic Gaia emerges. As you know, I have been defending a Gaia theory that identifies the biosphere with a living organism for about two decades now, but it is very difficult to publish something like that in the scientific field. When you are situated in this new paradigm, many of the controversies that are dealt with in biology, ecology and natural philosophy are quickly interpreted in a different way, sometimes in a very simple way.

The case at hand has been under discussion in evolutionary biology for many decades, although with a tendency not to go into it in depth. From my publications on the organic Gaia theory in which some of this is described and explained, I was encouraged a couple of years ago to write a brief article that tried to explain two ideas. Firstly, that the rate of appearance of the MTE in the hierarchy observed on Earth did not fit with the classical explanations from evolutionary biology. Secondly, that from the physics and Prigogine’s interpretation of complex dissipative systems could have a coherent explanation. As had already happened to me on many occasions since the 1990s, history repeated itself: I submitted the article to some relevant journals and the editors did not even take it for review. After three rejections, it occurred to me to ask for help and go to a recognized biologist who could share my ideas. I felt that the most advanced was Dan, since he already had graphs showing an acceleration in complexity and hierarchical levels and had been studying the subject for some time. I sent him my work and he enthusiastically offered to help me. The help quickly turned into collaboration and a lot of discussion of details and, above all, an impressive improvement of the article. Its length and quality were elevated, and also its language was “translated” to one closer to that of biology. I would also emphasize that this transdisciplinary discussion with Dan led me to a greater conviction of the role and meaning of Prigogine’s trinomial, to deepen the literature on the details and to rectify the certain prejudice I had with bryozoans, the first colonial animals, perhaps because of the fascination I have for social insects (bees, termites and ants) and because at first I thought it could unbalance my idea that we were following an exponential curve. I must also say that Dan is a biologist with a very keen phenomenological sense of thermodynamics —e.g. it was he who wrote the example of the hurricane given in the article. I think it was necessary to have a biologist with a good phenomenological knowledge of physics, and vice versa.

Dan: When Carlos approached me with an offer to collaborate, I saw a wonderful opportunity to explore some ideas I’d had about the relationship between far-from-equilibrium systems and large-scale evolution with a physicist who had also thought about these things. It was an opportunity to learn, but I didn’t expect us to agree on much. Most of my attempts to explore this area with physicists hadn’t gone very far, because we were unable to get past differences in fundamental concepts. This collaboration with Carlos worked out very differently. It turned out we were thinking about these problems in roughly the same conceptual terms, and our differences mostly boiled down to differences in terminology. Carlos is a physicist who can — when the occasion calls for it — think like a biologist! It also emerged that his view offered a new way to think about a problem I had been wrestling with for some years, the acceleration over the history of life in the origin of new levels of organization, the rise in hierarchy from bacterium to eukaryotic cell to multicelled individual to colony. I had a tentative solution that I’d proposed in a previous paper but Carlos enabled me to see it in far more general terms, in a way that encompassed more than the biological details of the trend.

2. Can you summarize for us what the main novelty of the paper is and why you think it is relevant in evolutionary biology and perhaps beyond MTE?

Carlos: I would say that the greatest novelty is the feedbacks between the elements and the whole that emerges from the interaction of the elements. Biology, like other sciences, has historically tended to a reductionist view, that is, to explain the details, such as the interaction of atoms – or of the minimal elements of each discipline: molecules in chemistry, genes in biology, etc. Prigogine asserted that even in physical systems, history is relevant and the formation of macroscopic systems, formers of history and wholes, not only emerges from microscopic interactions but also in the process of formation as well as once the whole is formed. That is, causation phenomena occur in the other direction: the whole also determines the microscopic processes that will be selected. This ends up generating a circular causality with great evolutionary potential and, under certain conditions, explosive, exponential. That is to say, there would be a top-down causation, from the highest level to the lowest, from what Prigogine calls structure to functions or microstructures. It is not that the whole has properties beyond the sum of the parts, it is that it ends up, in certain systems, determining the interaction of the parts. Prigogine thought he observed this in certain physical systems and argued that it could be applied to biological and social systems. I took him seriously.

The result is that this cycle of causation (in which the third element of the trinomial is fluctuations, which I interpreted as the flows of energy and matter between systems) has an evolutionary potential in the case of biology that can result in acceleration of the processes under study. That is, exponential functions that appear when there are positive circular feedbacks. Without this “force”, evolutionary biology was struggling to explain why it seems that certain processes of complexity, such as the MTE, accelerate, considering that from classical theories what is expected is a slowdown in evolution. Furthermore, in this trinomial view, it is shown that it requires phases that from the micro perspective we interpret as the necessary collaboration of entities —in the case of biology, organisms. This would explain that the most relevant thing in evolution is not competition but cooperation as a way to solve problems, but as a universal tendency affirmed by physics itself!

If we place ourselves in the perspective of the wholes formed there would exist a tendency towards the formation of wholes in evolutionary systems and those wholes would promote the cooperation of their parts, coordinating them. Again, with support in the thermodynamic laws. This is shocking, because thermodynamics would be teaching us just the opposite of how it was interpreted in much of the nineteenth and twentieth centuries, as that tendency to degradation. And it turns around a certain historical obsession in evolutionary biology since Darwin to interpretations of struggle and exclusive competition that has often had an impact on how we have organized ourselves socially, economically and morally in recent centuries. Of course, in the article we try to touch only on some of these issues, as it can be quite controversial to focus on something so specific.

Dan: I fully endorse Prigogine’s and Carlos’s top-down view of causality. It is a view that has been implicitly present but officially absent in evolutionary discourse. Officially, causation run upward, bottom-up, starting with the genes and ending with the organism and its ecology. Implicitly, however, Darwinian natural selection is necessarily a top-down process. It is — in the words of the 20th century paleontologist Leigh Van Valen — “the control of development by ecology.” An ecological entity acts downwardly on the organisms it contains, filtering out the less adapted variants, encouraging the better adapter ones, and moving populations toward toward greater fitness.

Interestingly, Carlos and I would express this sort of causation in somewhat different terms. In his terms, the whole determines the lower-level processes that are selected. In mine, the lower-level processes are not determined but arise randomly, as traditional theory says, and those variants that support or encourage the flow of energy through the system are stabilized by the whole, or in standard Darwinian terms are “selected” or “favored.” In both ways of expressing this, the causal arrow runs downward from the higher level system (in biological terms, ecology) to its parts (organisms or lineages).

3. What do you mean by “de-Darwinization” or “machinification” of parts and what does this process entail in the evolutionary literature?

Carlos: Scientific literature has identified terms like de-Darwinization, machinization or domestication when the wholes formed at the level of the hierarchies we describe subtract capacity of autonomy to their parts that were once “fuller” wholes (organisms): bacteria that are incorporated into the eukaryotic cell and end up as an organelle such as the chloroplast or the mitochondrion, cease to be so autonomous, lose functions (and genes) and are thus machinized or domesticated by that whole. Natural selection no longer acts on the mitochondrion as it did on the bacterium, it would act on the eukaryotic cell, in this sense, evolutionary biologists speak of de-Darwinization. So that we do not think of this process in an excessively anthropomorphic way, I usually use —although we have not incorporated it into the article— “telos transfer”: the whole absorbs the functions, the purposes, the autonomy (coordinates) of the parts, which in their day were directed towards themselves. I also speak of “dilution of egos”, the egos when collaborating and cooperating with others are forming wholes and are diluted as egos in front of the new ego that is being formed. But these terms are too radical for a biology still anchored in reductionist mechanicism, where teleological schemes (not necessarily self-conscious) are mercilessly attacked, although common sense tells us that when a bird builds a nest it does so with a purpose (teleology) that belongs to it and emerges from the bird.

Dan: In a paper some years ago, I described what I called a “complexity drain” that occurs in the evolution of higher-level individuals. The paper arose from a casual observation that cells in multicellular individuals seemed to have fewer parts than free-living single-called organisms. A skin cell in a mammal has fewer parts — fewer organelles and fewer internal structures generally — than an Amoeba. Indeed some cells in multicellular organisms, such as human blood cells, have no macro-scale parts at all. So I set out to test this, developing an objective and operational definition of a “part” and using electron micrographs in the literature to count cell parts. The data strongly supported the existence of a drain. In evolutionary terms, the drain makes sense. As Carlos says, with the emergence of a multicellular individual, some of the various functions that the organism must perform are transferred from the cells to the multicellular whole. A liver cell does not need to collect oxygen or food, nor does it need to reproduce, because these functions are accomplished by the multicellular whole. Thus the liver cell needs fewer parts. Thinking about it further, it seems quite likely that the same evolutionary logic applies across all levels, that the emergence of the eukaryotic cell produced a drain on parts within the prokaryotic cells within it. And the emergence of societies and colonies produces a drain on the parts within the multicellular individuals that compose them. These last two almost certainly occurred but have not been demonstrated formally with robust data sets: an opportunity for some empirically minded biologist.

4. So you both deal with the topic of complexity and its evolution. To what other fields beyond the case of MTE do you think your discussion would be relevant?

Carlos: I had relied on the same ideas to speculate that the trend in the complexity of organisms, measured somehow by the minimum number of genes to “make” an organism, followed an exponential function rather than a slowing increasing function as would be expected from classical theories in biology. In fact, I tried to publish it at the time, without reference to Prigogine’s trinomial. The problem is that the number of genes is a weak way to measure complexity and on the other hand, the fuss is impressive because the functionality of genes is not at all direct to their number. I am now thinking more of a study that identifies the number of protein variants (proteomics), something I would invite microbiologists reading this to explore. In any case, the minimum number of genes to make a bacterium, an eukaryotic cell, a simple multicellular organism such as a sponge or a jellyfish and a complex organism such as a leopard, if you put it in terms of the geological time it took for them to appear for the first time, also correlates with an accelerated function while the classical theory would still predict a slowdown.

Dan’s work precisely convinced me that it was better to explore hierarchical breaks. But for me, the most relevant thing is that there is a directing force, a physical tendency, which would help to explain why from a formless soup —thus our Universe was born— increasingly complex structures are formed under certain conditions in an accelerated way (although with limits) and in the case of biological phenomena, if we contemplate ecosystems and Gaia from Prigogine’s scheme, we can also infer processes of functions transfer, of machinization and coordination, which we said before, from all that we would call ecosystem and Gaia. I believe that ecology would turn around if treated in this way, and Gaia theories as well, because they could explain their phenomena from these wholes without always and exclusively resorting to micro phenomena, ultimately to quantum physics. It is somewhat paradoxical that it is physics that thus defends that the biological and social sciences make full sense, that they do not have to lose their work because the reductionist project towards atomic physics is impossible.

Finally, I point out a couple of ideas that are in the footnotes of the article, but which I think could be relevant. On the one hand, colonial animals is not necessarily the end of the story, if we are still in the exponential phase, it is quite possible that there are no limiting factors already present that prevent further up the hierarchical chain, and in turn, the colonies have a great future path, a guaranteed success, they will be invented more times and will evolve in internal complexity. That is consistent with what we describe, and exciting. In turn, if we extrapolate the chain to the past, we say that the first bacteria did not have material time to form on Earth, from which it follows that we would be showing, I think for the first time, a theory that would discriminate between two hypotheses: that the origin of life occurs on Earth or that the origin is extraterrestrial, older than the Solar System and that the Earth was colonized by extraterrestrial bacteria. Until now I believe that there was no theoretical basis for preferring one or the other, hence both were explored, although mostly the “wrong” one in my opinion. On the other hand, many of the evolutionary processes of functional losses, genetic losses and so on, of ecosystem level scales, would find an explanation from our discussion of MTE processes using the same theoretical scheme. Thus, that we do not synthesize vitamin C is part of a process of telos transfer, to larger wholes, functional anchoring to the ecosystem and to Gaia….

Dan: Carlos and I are agreed on most of what he says. One point of departure, though, has to do with the expectation for future hierarchical evolution. The social level — individuals collaborating to form societies — formed and stabilized at least 480 million years ago (with the origin of the first advanced colonies of bryozoans, which form coral-like colonies). These are the first “superorganisms.” Since then, no unambiguous super-superorganisms have evolved, I would argue. Humans are highly social, of course, but our highest-level associations of societies — nation states, and meta-societies of various kinds — are relatively weakly integrated. A nation state can have enormous power and capability but it is not an organism, in my view. (Carlos and I had a number of fascinating discussions about what it takes to qualify as an organism!) Anyway, if I am right, and if no super-superorganisms have evolved in the last 480 million years, it raises the possibility that the trend instantiated by the major transitions has reached its upper limit. As Carlos and I argue in the paper, all far-from-equilibrium systems have such limits. Most simple physical systems reach their upper limit with only a small number of nested levels of trinomials. Organisms, owing to their complexity, can form deeply nested systems. But even they have limits.

5. In the article, certainly, both of you connect at the end, in a relatively brief way, with the Gaia theory and in particular you timidly open theto a quantitative discussion of the degree of its organicity. To what extent is what both of you expose compatible with the organic Gaia theory proposed by Carlos?

Carlos: It is not only compatible. As I have explained in other places, the organic Gaia theory tries to find the “mechanisms” that lead to its emergence, to the emergence of a macrosystem in the biosphere with the same characteristics as a living organism, a living being. One of these mechanisms is the same process that we described in detail in the article: initial cooperation directed by the thermodynamics of complex dissipative systems that leads to the formation of structures, in turn thermodynamics would give a greater probability of forming and maintaining these structures and the capacity of these structures to first influence and then coordinate their parts -organisms-, and finally, the formation of an organic whole.

The other great explanatory aspect that we did not go into in the article, which has to do with the need to recycle materials, would help in the case of biological systems to end up forming an organic Gaia. But once formed, and in coherence with Prigogine’s trinomial, Gaia is who coordinates, who “domesticates” the organic whole that establishes the top-down relationships that will direct the internal processes, including the internal evolution of what we call organisms and their MTE. In addition to what has been described, I believe that the acceleration observed in the MTE needs the support of a complex and organic whole such as Gaia, because the barriers and limiting factors to this evolution are very large.

Dan: When it comes to Gaia, I am more timid than Carlos. In particular, I am reluctant to call it an organism. The reason is that I am uncomfortable with terms suggesting dichotomies, uncomfortable with either-or, in biology. In standard thinking, organism-ness — or as Carlos has felicitously called it, organicity — is generally understood as a dichotomous concept. Either something is an organism or it is not. There are debates in biology about whether, say, a virus is an organism or not, but in most of these the standing assumption is that organismness is not a matter of degree. I think that in biology, very few things are all-or-none, very few things are discrete. In mammals, for example, not even number of arms is discrete. (Consider individuals conjoined at birth.) And I’m guessing that organismness is not going to turn out to be discrete. When we understand biological systems better, my guess is that we will be able to devise an organism-ness scale with multiple variables — like capacity to reproduce and capacity to metabolize and so on — and that each biological entity, from viruses to Gaia, will register as an organism to some degree, more or less, on each of them. Anyway, our debate on this issue — the organism status of Gaia — was for me one of the most interesting discussions we had!

6. And could you point out any implications of your contribution beyond biology, e.g. in anthropology, philosophy…?

Carlos: I do not know if it is my role as a scientist to point out these implications, although as a person, I clearly see them. It is not the same to treat all living beings as “complex mechanisms” than to give them a more “living” character, with qualitative value, especially if Gaia is alive. If we consider that Gaia is an organism, the rest of living beings are part of it, and the sustainability of the Gaia organism and its parts depend on the proper functioning of its parts. It seems an approach that leads us to wonder whether our society, in recent generations, is not behaving in a way analogous to a cancer. But it certainly breaks with an excess of anthropocentrism, and our article in particular tends to break also with that myth that we are selfish in a world of competitive struggle from biology: there is a physical bias towards cooperation. I believe that biology, recognizing collaboration or mutual aid, now has more support for these relationships to emerge from anecdotes that need to be explained. Darwin himself already used many more examples of exclusionary competition than of altruistic cooperation.

What if we turn the usual discourse around and try to explain competition as anecdotal, as opposed to the general cooperative tendency? Not long ago I read an article about bonobos, which showed that they have xenophilic tendencies (“love for the stranger”, something interesting to form all more comprehensive), to a large extent they had to justify it very well and with excessive explanatory ornaments, something that seems only necessary when the paradigm is competitive and fierce struggle for survival. It does not surprise me, indeed, it is the “natural” thing to do in such a complex organism.

Dan: Before my collaboration with Carlos, I had not thought much about the social or political implications of this issue. And I am indebted to him for our discussions, which to large extent brought me around to his view. Yes, the Prigogine view supports a less competitive, more cooperative view of the biological world. The higher-level system, our ecology, reaches down into its parts (us) and stabilizes interactions that support the flow of energy through the system, and many of these stabilizing interactions are likely to be cooperative. On the other hand, let us not forget the complexity drain, the machinification, that also occurs. We should expect that the higher-level social whole will favor the removal of “parts” within us, the stripping of excess capacities at the individual level, functions that the whole performs better and more effectively. Ant colonies are “smart” in some sense, but that intelligence is possible in part because their component individuals are “stupid.” That is, individual ants have been stripped of much of their complexity and autonomy. Applied to humans, the complexity drain means that social intelligence comes with the same cost, a reduction in complexity and autonomy at the individual level. It’s not hard to imagine contrasts that make this point: a human hunter gatherer could be omnicompetent, in the sense that every individual is able to understand and perform most essential tasks. I, on the other hand, am doubtful of my ability as an individual to grow enough food to feed myself for a whole year and am somewhat over my head when I turn on my car.

7. What reception do you expect from this work in your respective academic fields and in what aspects would you like to further develop this research in the future?

Carlos: The truth is that I expect more impact outside physics and biology, at least for now. In physics it took centuries to move from the mechanicism, determinism and reductionism initiated by Newton to the physics of the 20th century that opened up to other paradigms from relativity, quantum, non-equilibrium thermodynamics and chaos theory. I suppose biology requires time, it has already been 150 years in a paradigm that physics made obsolete (although not necessarily physicists), perhaps it still has decades ahead to “imitate” the path followed by physics, I hope not many, as I would like to experience it in life. As for future work, it will partly depend on whether there is reaction and which one to the article. I would love to continue to abuse Dan’s knowledge and common sense, but we both don’t have much time right now. There is also a project that is older than this, which I even consulted with Prigogine himself in the 90’s, the idea that the very mechanisms used by evolutionary biology (neo-Darwinism more specifically), do not comply with Prigogine’s trinomial (no top-down causation, for example). He thought he understood it that way when I told him about it, but he did not want to get into the mess, although he encouraged me to do so. I doubt that I would encourage to do so after decades of fruitlessness, and I think it is more practical to try to expose the Gaia theory that I defend with its two basic pillars without attacking neo-Darwinism, now that there is already one of them with an example exposed and perhaps admitted.

Dan: I am more optimistic about the impact on biology. Evolutionary biology, at least, has moved on from neo-Darwinism in recent decades. The so-called “modern synthesis” is no longer the state of the art. Instead we have been debating what form an “extended synthesis” will take. No consensus has been reached, of course, but it is clear that top-down causation, thermodynamics and Prigogine-style thinking, and even a somewhat-living Gaia will be much more welcome in the newly developing discourse. And I think our paper will be considered an important contribution to that discourse. As for future research, I have been working over the past decade on a new way to understand goal-directedness or purpose, one that applies to all goal directed systems, from a bacterium following a food gradient to goal-directed machines to affective processes like wanting and preferring in animals that have those capacities. Intuitively, far-from-equilibrium dynamics should be part of the complete story, although — despite having learned an enormous amount from Carlos (thank you, Carlos!) — I am not enough of physicist yet to tell that story. Working on it.

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