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Holobionts: a new Paradigm to Understand the Role of Humankind in the Ecosystem

You are a holobiont, I am a holobiont, we are all holobionts. "Holobiont" means, literally, "whole living creature." It ...

Saturday, June 25, 2022

Survival of the fittest or non-survival of the unfit? How the theory of evolution has evolved.

Lynn Margulis, one of the brightest minds of the 20th century, developer or co-developer of concepts such as "Gaia", "endosymbiosis," and "holobiont." Image from Gabriela Govantes Morales

Life did not take over the world by combat, but by networking.

Lynn Margulis

The first study in the field we call today the “science of complex systems” was Darwin’s synthesis of evolution by natural selection, in 1859 1. Initially, Darwin’s ideas were often understood as implying mainly competition (“Nature in red tooth and clay”). Nowadays, we tend to emphasize more the concept of collaboration, often in terms of the concept of “symbiosis” and of the paradigm that goes under the name of “holobiont,” an ensemble of creature that live together in a condition of symbiosis.

“Holobiont” is a term known from the 1930s 2, but the idea of collaboration among living beings, microorganisms in particular, is much older. It may go back to the concept of “consortia” developed in mid 19th century 3. Nowadays, it is mostly associated to the work of Lynn Margulis, who used it starting with the 1990 4 5, although she had been studying the subject already in the 1960s 6. The interest in holobionts has been rapidly growing with the 2000s 2 and that led to a variety of different interpretations of what exactly a holobiont is. Here, I am not even trying to provide a comprehensive discussion of the many ways in which the holobiont concept is interpreted. Let’s say that the holobiont term can be seen as a meme growing in the memesphere 7 and, true to its evolutionary background, has been following a memetic evolutionary path, changing and adapting as its memetic environment changes.

The most common interpretation sees holobionts in a relatively narrow sense, as systems formed by a host organism and its associated symbiotic micro organisms, e.g. the gut bacteria of human beings (see, e.g. the work by Rosenberg 8. We can call this the “classical” view that focus on host-microbe interactions. A more general definition is provided by Castell and others 9, 10 in terms of the concept of “complex adaptive systems” (CAS) 11. CAS systems are formed of a network of elements (“nodes”) which, in this case, may consist of individual organisms or smaller holobionts, thus making the definition “fractal” or “self-similar.” The highest rank holobiont of the ecosystem is the ecosystem itself, that some call Gaia 12), 13.

The nodes (the creatures) of the holobiont network are connected to each other by flows of matter, energy, or information and are affected by “feedback” phenomena. The term “feedback“ indicates a condition that makes the flow proportional (or inversely proportional) to the status of the nodes they are connected to. It is the interplay of feedbacks that stabilizes the system and makes it tend to reach homeostasis. CAS systems have several typical characteristics, one is of reacting to perturbations by damping them and trying to maintain their state and reach the condition called “homeostasis.”

Castell et al. use the term “Holobiont-like system” (HLS) for these CAS systems that they describe as biological systems. In this paper, I’ll use the term “holobiont” as a general term that includes HLSs and I will argue that the “network” characteristics of these systems makes the definition applicable to non-biological systems, e.g. social and economic networks.

One characteristic of CAS is their capability to evolve. It is embedded in their tendency to react to external perturbations (called “forcings” in the jargon of system science) in order to attain homeostasis. Those systems which can do that tend to persist for a long time, so they are winners at the evolutionary game. But there is more to the concept of holobiont: it can be used to explain how evolution moves in steps by co-opting of different creatures in a single organism 6. According to Margulis 5, the unit of evolution is not the genome of individual organisms, but the “hologenome,” the ensemble of the genomes of the creatures that compose a holobiont. This concept is not without problems, in particular about what are the boundaries that define a specific holobiont, but it is gaining acceptance in the scientific community 14, 15.

The present paper is a review of the concept of “holobiont” aimed at developing mental tools helping us to understand how and why many complex systems around us exist and operate. The “holobiont paradigm” can help redress our views of the world and lead us to take a more collaborative attitude toward nature and our fellow humans. It is a way to change our current way of thinking and transform it into a gentler and more balanced view of the world, where we take what we need from Nature and give back to Nature what Nature needs. And the same concept holds for human life in human society.

Holobiont: how evolution has evolved

A well-known poem by Tennyson mentions “Nature in Red Tooth and Claw.” It was written in 1850, before Darwin’s book, “The Origin of Species”(1859), appeared in print. But, in time, Tennyson’s sentence started to be seen as embodying the very essence of Darwin’s ideas. It implied that the natural world is a continuous fight where the best individuals prevail and reproduce, while the others leave no descendants and disappear. During the 19th and 20th centuries, Darwin’s ideas were often coerced into a version that considered evolution as not a purely random phenomenon, but a purposeful motion toward creating species of higher and higher perfection 16. This distorted interpretation of Darwin’s ideas percolated into fields other than biology. Competition is often seen as the key element that makes it possible for people to become better at their jobs, for technology to improve, for companies to produce better products, and more. Even sports are always supposed to be competitive: from the time of Baron De Coubertin, we accept that we should let the stronger win the battle and the swifter the race (even though the Ecclesiastes book says otherwise). During the 20th century, distorted versions of Darwin’s theory were used to justify all sorts of crimes against humankind. Darwin himself would have been horrified if he had known that his ideas would have been used in this way.

The idea of the “survival of the fittest” is not wrong, but it has created a lot of confusion about how exactly natural selection works. Darwin emphasized the survival of the fittest because of his reliance on human breeding of domesticated animals and plants as examples. Human-led selection is focused on forcing species to acquire one or a few specific characteristics that humans find useful. The results are optimized, but only for that characteristic, often at the expense of many others that are needed for survival in the wild. Horses can be optimized for their ability to run, donkeys for their ability to carry weights, grains for the size of their eaves, apples for their taste and size, and there are many more similar cases. But most of the creatures optimized by humans would not survive for long in the wild. It is similar to the mitochondria in eukaryotes, which could not survive outside the larger cells they populate. Individual organisms rarely survive alone: mostly they are part of groups (herds, flocks, prides, etc.) that provide shelter, protection, and more. A fitter animal still needs to be part of a group, and that limits the advantage of being special. Rather than for the fittest, evolution strives for the not so bad.

An example. Think of a herd of wild zebras. The paradigm of “survival of the fittest” implies that zebras continuously evolve toward fitter and fitter creatures. Predators which attack zebras do the same. The result is called, sometimes, the “evolutionary arms race” between prey and predators 17. If we understand evolution at the individual level, we can imagine that it would result in creating a "super-zebra" that can run faster than the other zebras. Would that give it an evolutionary advantage?

We may not be so good a thinking like zebras, but it seems obvious that, for a zebra, survival is mostly guaranteed by being part of the herd. The herd will not directly fight back against predators (although in some cases it will, it is called "mobbing"), but it will provide early warning of the presence of predators, its movement will confuse them and single zebras will have a statistically better chance of survival. An isolated zebra has no chances to escape once it is the target of a group of predators, so being able to run very fast is probably a negative characteristic, especially considering that it could only be obtained at the expense of other useful characteristics, say, endurance, metabolic efficiency, or others. On the opposite side of fitness, instead, evolution works by removing the unfit. Clearly, zebras that cannot follow the herd are a preferred target for predators and their genes are removed from the gene pool. It is natural selection at work

Overall, therefore, the herd will be formed of individuals of similar characteristics. It is a typical holobiont formed by a group of individual organisms linked to each other, in this case mostly by visual signals. No zebra aims at helping its companions escape predators, but once they get together, their chance to be killed is reduced. A typical example of symbiosis. There is no altruism in symbiosis, only individual advantage. But that individual advantage benefits the whole group. The “hologenome” of the herd, the set of individual genomes, is the unit of evolution.

Once we define evolution in terms of holobionts, we can take a different look at the mechanism of selection. Darwin used the terms “survival of the fittest” and “natural selection” as nearly interchangeable ones, but that’s not the case. “Survival of the fittest” means that Nature selects in favor of the fitter creatures. “Natural selection,” instead, can be seen as meaning that nature selects against unfit creatures. The first interpretation (survival of the fittest) implies a continues evolution toward better and better fitness. The second (natural selection) implies a tendency toward stability or, using a more specific term, homeostasis.

The "removal of the unfit" is a fundamental concept. The biosphere, like any complex system, is subjected to an increase in disorder according to the 2nd law of thermodynamics. But the law applies only to isolated systems. The biosphere is not one, and it can keep entropy growth in check using natural selection to maintain homeostasis. The concept of evolution as the removal of the unfit was developed in particular by Gorshkov et al., 18 who put together a synthesis of how the ensemble of the living creatures on Earth (the biosphere) control the wider entity that we call the “ecosphere” generating the condition of dynamic stability we call “homeostasis.” This view was described in terms of the concept of “biotic regulation of the environment.” So, the biosphere does not normally aim at increasing the degree of fitness of individuals. The system strives for stability and the winners of the evolutionary game are those organisms which can best maintain it.

If stability is the aim of evolution, then, how does anything evolve at all? That is, how is it that Earth isn’t still populated only by marine prokaryotes, as it was during the Archean, billions of years ago? The holobiont paradigm helps resolve this problem, too, taking into account the phenomenon of “endosymbiosis,” the true motor of evolution.

Darwin’s ideas about evolution involved gradual and continuous change. The modern paradigm, called “neodarwinism” is based on molecular biology and assumes that evolution occurs as the result of modification of the genetic code of organisms, the result of either random mutation or sexual mixing (meiosis). In other words, evolution is a continuous “probing” of the fitness of organisms, where those better adapted at survival pass their genes to their descendants.

Yet, this interpretation has a problem. The gradual change of the genetic code can hardly account for the discrete evolutionary “jumps” needed to go from one species to another. This question was termed the “irreducible complexity problem” 19, and sometimes it was understood as implying the need to admit a supernatural intervention (“intelligent design”) to explain some features of living beings. A classic example is that of eyes. How could ancient, blind animals, develop eyes?

It is hard to find for eyes the same evidence of a gradual evolution that Darwin had observed for the beaks of finches in the Galápagos Islands. The first multicellular animals appeared at the time of the “Ediacaran Fauna” (also known as “Vendobionts”), some 600 million years ago. There is no evidence that these creatures had eyes. Instead, fully formed eyes clearly appear in the early Cambrian biota, starting from about 520 million years ago 20. So, we have this new evolutionary invention, eyes, that appear relatively suddenly, already in a functional form. How could it happen?

Attempts to solve the problem by postulating gradual steps were only partially successful. For instance, in 1994, Nilson and Pelger 21 proposed that a flat, light-sensitive surface could naturally turn into an eye-like optical structure in a few hundred thousand years of gradual evolution. It may be a correct estimate, but where did the light-sensitive surface come from? What benefit could early animals have from such a capability?

The concept of endosymbiosis gives us a way to explain this and many more evolutionary rapid changes. Endosymbiosis assumes that multicellular creatures are collections of formerly independent unicellular organisms. We may assume that early multicellular organisms co-opted microorganisms that had developed the stigma, a feature still present in some modern microorganisms. The stigma is a pigmented area in the cell connected to photoreceptor molecules. These molecules directly act on the flagellum (the “tail” of the creature). In this way, the microorganism can detect light and move toward it. It is typical of a creature called euglena, a protist that is both plant and animal. It uses photosynthesis – hence it is a plant – but it also moves, a characteristic of animals. There is no doubt that having a photosensitive receptor gives to the euglena an evolutionary advantage: it can move toward the light, which it needs for its photosynthetic activity. Light-sensitive microorganisms (not necessarily the euglena, which is a modern organism) give us the key to solve the “irreducible complexity” problem. Animals didn’t need to develop eyes from scratch. They borrowed light-sensitive organs by entering into a symbiotic relationship with unicellular creatures that had developed them. Later, they gradually turned these light-sensitive layers into organs able to form an image of the external world -- the organs we call “eyes.” This point is very general and another example of the usefulness of the concept of “holobiont”. There are many issues in evolution that cannot be solved unless we recur to the concept of endosymbiosis.
This point is very general. There are many issues in evolution that cannot be solved unless we recur to the concept of endosymbiosis. For another example, note how there are no intermediate species between prokaryotes (simple cells with no organelles) and eukaryotes (complex cells, with internal organelles) Nick Lane wrote a fascinating book in 2015 titled “The Vital Question,” (Lane 2015) dedicated to the attempt to explain why it is so. Clearly, we have another problem of irreducible complexity that can only be explained if we assume that what we call “organelles” are formerly independent organisms that were fagocitated by a larger cell and became part of it. This process is the basis of the concept of holobiont as proposed by Lynn Margulis (Sagan 1967), (L. Margulis 1975).

Once we define evolution in terms of holobionts, we can take a different look at the mechanism of selection. Darwin used the terms “survival of the fittest” and “natural selection” as nearly interchangeable ones, but that’s not the case. “Survival of the fittest” means that Nature selects in favor of the fitter creatures. “Natural selection,” instead, can be seen as meaning that nature selects against unfit creatures. The first interpretation (survival of the fittest) implies a continuous evolution toward better and better fitness. The second (natural selection) implies a tendency toward stability or, using a more specific term, homeostasis. It means that individuals seek for collaboration rather than competition -- a basic characteristic of holobionts. The winners of the evolutionary game are always good holobionts!


1. Charles Darwin. The Origin of Species. (John Murray, 1859).
2. Baedke, J., Fábregas‐Tejeda, A. & Delgado, A. N. The holobiont concept before Margulis. J. Exp. Zoolog. B Mol. Dev. Evol. 334, 149–155 (2020).
3. Kull, K. Ecosystems are Made of Semiosic Bonds: Consortia, Umwelten, Biophony and Ecological Codes. Biosemiotics 3, 347–357 (2010).
4. Margulis, L. Words as battle cries—symbiogenesis and the new field of endocytobiology. BioScience 40, 673–677 (1990).
5. Margulis, L. Symbiotic Planet: A New Look At Evolution. (Basic Books, 2008).
6. Sagan, L. On the origin of mitosing cells. J. Theor. Biol. 14, 225-IN6 (1967).
7. Dawkins, R. The selfish gene. (Oxford ; New York : Oxford University Press, 1976).
8. Rosenberg, E., Koren, O., Reshef, L., Efrony, R. & Zilber-Rosenberg, I. The role of microorganisms in coral health, disease and evolution. Nat. Rev. Microbiol. 5, 355–362 (2007).
9. Castell, W., Fleischmann, F., Heger, T. & Matyssek, R. Shaping Theoretic Foundations of Holobiont-Like Systems. in Progress in Botany 77 (eds. Lüttge, U., Cánovas, F. M. & Matyssek, R.) 219–244 (Springer International Publishing, 2016). doi:10.1007/978-3-319-25688-7_7.
10. Matyssek, R., Lüttge, U. & Castell, W. Evolution of Holobiont-Like Systems: From Individual to Composed Ecological and Global Units. in Progress in Botany 1–46 (Springer, 2022). doi:10.1007/124_2022_57.
11. Mobus, G. E. & Kalton, M. C. Principles of System Science. (Springer, 2015). doi:10.1007/978-I-4939-1920-8.
12. Matyssek, R. & Luttge, U. Gaia: The Planet Holobiont. Nova Acta Leopoldina 114, 325–344 (2013).
13. Castell, W., Lüttge, U. & Matyssek, R. Gaia—A Holobiont-like System Emerging From Interaction. in Emergence and Modularity in Life Sciences (eds. Wegner, L. H. & Lüttge, U.) 255–279 (Springer International Publishing, 2019). doi:10.1007/978-3-030-06128-9_12.
14. Gray, M. W. Lynn Margulis and the endosymbiont hypothesis: 50 years later. Mol. Biol. Cell 28, 1285–1287 (2017).
15. Morris, J. J. What is the hologenome concept of evolution? F1000Research 7, F1000 Faculty Rev-1664 (2018).
16. Bowler, P. J. The Non-Darwinian Revolution: Reinterpreting a Historical Myth. (Johns Hopkins Univ Pr, 1992).
17. Dawkins, R. The Blind Watchmaker. (Norton & Company, 1986).
18. Gorshkov, V. G., Makarʹeva, A. Mikhaĭlovna. & Gorshkov, V. V. Biotic regulation of the environment : key issue of global change. (Springer-Verlag, 2000).
19. Behe, M. J. Darwin’s Black Box: The Biochemical Challenge to Evolution. (Simon and Schuster, 2001).
20. Zhao, F., Bottjer, D. J., Hu, S., Yin, Z. & Zhu, M. Complexity and diversity of eyes in Early Cambrian ecosystems. Sci. Rep. 3, (2013).
21. Nilsson, D. E. & Pelger, S. A pessimistic estimate of the time required for an eye to evolve. Proc. Biol. Sci. 256, 53–58 (1994).
22. Jensen, K. H. & Zwieniecki, M. A. Physical Limits to Leaf Size in Tall Trees. Phys. Rev. Lett. 110, 018104 (2013).

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