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 (Charles Darwin 1859). 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 the paradigm that goes under the name of “holobiont,” an ensemble of creatures that live together in a condition of symbiosis.
“Holobiont” is a term known from the 1930s (Baedke, Fábregas‐Tejeda, and Delgado 2020), but the idea of collaboration among living beings, microorganisms in particular, is much older and it may go back to the concept of “consortia” developed in mid 19th century (Kull 2010). Nowadays, it is mostly associated to the work of Lynn Margulis, who used it starting in the 1990 (Lynn Margulis 1990) (Lynn Margulis 2008), although she had been studying the subject already in the 1960s (Sagan 1967).
The interest in the concept of holobiont has been rapidly growing with the 2000s (Baedke, Fábregas‐Tejeda, and Delgado 2020) and that led to a variety of different interpretations of what exactly a holobiont is. Let’s say that the holobiont term can be seen as a meme growing in the memesphere (Dawkins 1976) and, true to its evolutionary background, has been following a memetic evolutionary path, changing and adapting as its complex memetic environment has changed.
Here, I am not even trying to provide a comprehensive discussion of the many ways in which the holobiont concept is interpreted. Let’s just say that the most common interpretation sees holobionts in a relatively narrow sense, as the systems formed by a host organism and its associated symbiotic microorganisms, e.g. the gut bacteria of human beings (see, e.g. the work by Rosenberg (Rosenberg et al. 2007). We can call this the “classical” view that focuses on host-microbe interactions. A more general definition is provided by Castell and others (Castell et al. 2016), (Matyssek, Lüttge, and Castell 2022) in terms of the concept of “complex adaptive systems” (CAS) (Mobus and Kalton 2015). 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, which some call Gaia (Matyssek and Luttge 2013)), (Castell, Lüttge, and Matyssek 2019).
The nodes (the creatures) of the holobiont network are connected to each other by flows of matter, energy, or information 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 CASs 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 different creatures in a single organism (Sagan 1967). According to Margulis (Lynn Margulis 2008), 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 (Gray 2017), (Morris 2018).
The present paper is a review of the concept of “holobiont” aimed at finding a unifying concept that could give us the key to understanding how and why many complex systems around us exist and operate. The “holobiont revolution” 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.
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.
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 the 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.
Apart from politics, Darwin’s theory became more and more a cornerstone of biology, especially with the birth of modern molecular biology. The molecular interpretation of evolution became known as “neodarwinism,” based on the well-known concept that the information (the “blueprint”) of a living being is contained in its genetic code in the form of DNA molecules. The concept that information flows from the DNA to proteins, and not the reverse, is known as the “central dogma” of neodarwinism. Within this paradigm, evolution is supposed to occur in the form of changes in the genetic code. So successful was molecular biology that the term DNA became synonymous in common parlance with concepts such as “destiny”, “blood,” or “karma.” Evolution, then, was the result of changes in the DNA molecules passed from one organism to another caused by random mutation or sexual mixing (meiosis).
Yet, there remained a basic problem in the theory of evolution: the gradual change of DNA molecules as the result of mutation or meiosis can hardly account for the discrete jumps needed to go from one species to another. This problem was sometimes described in terms of “missing links” supposed to relate modern humans to their remote ancestors. Of course, the missing link is just an invention of the media -- it does not have a scientific basis. Yet, there are features in living beings that are difficult to understand in terms of a gradual process of natural selection, as Darwin described it. A classic example is that of eyes. How could ancient, blind animals, develop eyes?
Indeed, 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. So, we have this new evolutionary invention, eyes, that appear relatively suddenly, already in a functional form. How could it happen?
This question was termed the “irreducible complexity problem” by Behe et al., and sometimes it was understood as implying the need to admit a supernatural intervention to explain some features of living beings. Attempts to solve the problem by postulating gradual steps were only partially successful. For instance, in 1994, Nilson and Pelger 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 evolution of eyes gives us another window on the concept of holobiont and the related concept of endosymbiosis. According to this view, multicellular creatures are multicellular collections of formerly independent unicellular organisms that were co-opted to form a holobiont. Following this line of reasoning, we may assume that the 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 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 solving 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. 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.
References
Charles Darwin. 1859. The Origin of Species. John Murray.
———. 2008. Symbiotic Planet: A New Look At Evolution. 1st edition. Basic Books.
Zhao, Fangchen, David J. Bottjer, Shixue Hu, Zongjun Yin, and Maoyan Zhu. 2013. “Complexity and Diversity of Eyes in Early Cambrian Ecosystems.” Scientific Reports 3 (September). https://doi.org/10.1038/srep02751.