Information and individuality

David Krakauer, Nils Bertschinger, Eckehard Olbrich, Jessica C. Flack1, Nihat Ay, The information theory of individuality, Theory in Bioscineces, (2020). https://doi.org/10.1007/s12064-020-00313-7

Abstract

Despite the near universal assumption of individuality in biology, there is little agreement about what individuals are and few rigorous quantitative methods for their identification. Here, we propose that individuals are aggregates that preserve a measure of temporal integrity, i.e., “propagate” information from their past into their futures. We formalize this idea using information theory and graphical models. This mathematical formulation yields three principled and distinct forms of individuality—an organismal, a colonial, and a driven form—each of which varies in the degree of environmental dependence and inherited information. This approach can be thought of as a Gestalt approach to evolution where selection makes figure-ground (agent–environment) distinctions using suitable information-theoretic lenses. A benefit of the approach is that it expands the scope of allowable individuals to include adaptive aggregations in systems that are multi-scale, highly distributed, and do not necessarily have physical boundaries such as cell walls or clonal somatic tissue. Such individuals might be visible to selection but hard to detect by observers without suitable measurement principles. The information theory of individuality allows for the identification of individuals at all levels of organization from molecular to cultural and provides a basis for testing assumptions about the natural scales of a system and argues for the importance of uncertainty reduction through coarse-graining in adaptive systems.

The architecture of individuality

From the perspective of physics and chemistry, biological life is surprising. There is no physical or chemical theory from which we can predict biology, and yet if we break down any biological system into its elementary constituents, there is no chemistry or physics remaining unaccounted for (Gell-Mann 1995). The fact that physics and chemistry are universal—ongoing in stars, solar systems, and galaxies—whereas to the best of our knowledge biology is exclusively a property of earth, supports the view that life is emergent. This stands in contrast to the universality of chemical phenomena which can be predicted from quantum mechanical considerations in fundamental physics even when this proves to be computationally cumbersome or intractable (Defranceschi and Le Bris 2000). The asymmetry in what can be gleaned from working down toward ever more elementary constituents versus working up through levels of aggregation is captured by the terms reductionism and emergence (Anderson 1972; Laughlin and Pines 2000). It is often difficult to predict physical properties of aggregates from knowledge of constituents, and this extends to questions of behavior where it is rarely clear how far “down” to go (Anderson 1972; Krakauer and Flack 2010a; Flack 2017b). There are assumed to be dominant microscopic scales for a given set of aggregate properties yet our understanding of what constitutes a fundamental unit (Gilbert et al. 2012; Daniels et al. 2016) and whether these units count as individuals, have implications for many areas of science, from taxonomy and cladistics through to physiology, behavior, and ecology (Clarke 2011; Wilson and Barker 2013).

It is almost inconceivable for us to imagine a biological science without a concept of units or individuality. After all, how could we speak about metabolism, behavior or the genome without first establishing a unit or container of observation and measurement? Even Schrödinger in his prescient book, What is Life? (Schrodinger 2012), sought to explore the persistence of biological phenotypes of organisms—or even features of ecosystems—through the lens of elementary and universal physical underpinnings, made strong prior assumptions about the reality of individual organisms:

“What degree of permanence do we encounter in hereditary properties and what must we therefore attribute to the material structures which carry them? The answer to this can really be given without any special investigation. The mere fact that we speak of hereditary properties indicates that we recognize the permanence to be of the almost absolute. For we must not forget that what is passed on by the parent to the child is not just this or that peculiarity...Such features we may conveniently select for studying the laws of heredity. But actually it is the whole (four- dimensional) pattern of the phenotype, all the visible and manifest nature of the individual, which is reproduced without appreciable change for generations, permanent within centuries—though not within tens of thousands of years—and borne at each transmission by the material in a structure of the nuclei of the two cells which unite to form the fertilized egg cell. That is a marvel.”

Schrödinger did not set out to derive the individual from fundamental physics but to reconcile existing and rather traditional conceptions of individuality (essentially the individual as synonymous with the observable organism) with the new physics of quantum mechanics.

In this respect, Schrödinger was adopting a typically reductionist perspective, explaining features of biological science through first principles of physics (Weinberg 1995). In Schrödinger’s case, the physical feature of greatest importance to biology was the long-lived covalent bond. But for many reasons this line of approach has failed to deliver the deep and unifying insights based on physics (Anderson 1972), from which powerful biological ideas—such as adaptation or individuality—might be derived (Dupré 2009; Keller 2009).

The question we seek to address is more limited. How do we identify individuals without relying on features like cell membranes that may be solutions to challenges faced by particular systems for maintaining integrity rather than foundational properties? We want to allow for the possibility that microbes and loosely bound ecological assemblages such as microbial mats and cultural and technological systems, when viewed with a mathematical lens, qualify as individuals even though their boundaries are more fluid than the organisms we typically allow. It may also be the case that entities currently considered individuals are indeed individuals but not in the way we think—organisms are more complicated than typical individuality definitions acknowledge. Humans for example contain approximately as many self-cells as symbiotic microbes (Andreu-Moreno and Sanjuán 2018), yet until recently with the advent of the concept of “holobiont” (Gilbert et al. 2012), the microbe portion of the human cellular ecosystem was not typically considered part of the human individual.

In an ideal case, visitors to an exoplanet would have a procedure for identifying or “perceiving” individuals based on a quantitative survey with minimal prior knowledge of the type of life form that they expect to encounter. In the next sections of the paper, we briefly review a few key standard assumptions about individuality in biology and challenges to formalizing the concept. We then discuss a way forward and develop an information-theoretic formalism.