Extensive social choice theory is used to study the problem of measuring group fitness in a two-level biological hierarchy. Both fixed and variable group size are considered. Axioms are identified that imply that the group measure satisfies a form of consequentialism in which group fitness only depends on the viabilities and fecundities of the individuals at the lower level in the hierarchy. This kind of consequentialism can take account of the group fitness advantages of germ-soma specialization, which is not possible (...) with an alternative social choice framework proposed by Okasha, but which is an essential feature of the index of group fitness for a multicellular organism introduced by Michod, Viossat, Solari, Hurand, and Nedelcu to analyze the unicellular-multicellular evolutionary transition. The new framework is also used to analyze the fitness decoupling between levels that takes place during an evolutionary transition. (shrink)

In this paper we explore the organizational conditions underlying the emergence of organisms at the multicellular level. More specifically, we shall propose a general theoretical scheme according to which a multicellular organism is an ensemble of cells that effectively regulates its own development through collective mechanisms of control of cell differentiation and cell division processes. This theoretical result derives from the detailed study of the ontogenetic development of three multicellular systems and, in particular, of their corresponding cell-to-cell signaling networks. The (...) case study supports our claim that a specific type of functional integration among the cells of a multicellular ensemble , is required for it to qualify as a proper organism. Finally, we argue why a multicellular system exhibiting this type of functionally differentiated and integrated developmental organization becomes a self-determining collective entity and, therefore, should be considered as a second-order autonomous system. (shrink)

We argue that the transition from unicellular to multicellular systems raises important conceptual challenges for understanding agency. We compare several MC systems displaying different forms of collective behavior, and we analyze whether these actions can be considered organismically integrated and attributable to the whole. We distinguish between a ‘constitutive’ and an ‘interactive’ dimension of organizational complexity, and we argue that MC agency requires a radical entanglement between the related processes which we call “the constitutive-interactive closure principle”. We explain in detail (...) that this is not possible without a regulatory center functionally integrating the two dimensions, and we also argue that, in turn, this type of regulation would not be possible without a special type of organization between the cells required for the development and maintenance of systems capable of integrated behavior. (shrink)

Since, it has become clear that individuality is not to be considered as a given, but rather as something which needs to be explained. How has individuality emerged through evolution, and how has it subsequently been maintained? In particular, why is it that multicellular organisms appeared and persisted, despite the obvious interest of each cell of favoring its own replication? Several biologists see the immune system as one of the key components for explaining the maintenance of multicellular organisms’ individuality. Indeed, (...) the immune system exerts a constant surveillance on all the constituents of the organism, including “cheaters” like tumor cells, which favor their own replication at the expense of the whole organism. In most cases, the immune system eliminates those cheaters. This is the “immune surveillance” hypothesis, first suggested by Burnet and Thomas. In this paper, I account for recent findings on immune surveillance in order to determine the precise role of the immune system in the emergence and maintenance of individuality. This investigation gives rise to a critical question for the domain of biological individuality: should immunity be considered as something unique to multicellular organisms? If it is indeed unique, should the multicellular organism be considered as an individual to a higher degree than any other living entity? If it is not unique, what precisely are the equivalents of the immune system in other living individuals? (shrink)

A crucial question for a process view of life is how to identify a process and how to follow it through time. The genidentity view can contribute decisively to this project. It says that the identity through time of an entity X is given by a well-identified series of continuous states of affairs. Genidentity helps address the problem of diachronic identity in the living world. This chapter describes the centrality of the concept of genidentity for David Hull and proposes an (...) extension of Hull’s view to the ubiquitous phenomenon of symbiosis. Finally, using immunology as a key example, it shows that the genidentity view suggests that the main interest of a process approach is epistemological rather than ontological and that its principal claim is one of priority, namely that processes precede and define things, and not vice versa. (shrink)

We review Evolution and the Levels of Selection by Samir Okasha. This important book provides a cohesive philosophical framework for understanding levels-of-selections problems in biology. Concerning evolutionary transitions, Okasha proposes that three stages characterize the shift from a lower level of selection to a higher one. We discuss the application of Okasha’s three-stage concept to the evolutionary transition from unicellularity to multicellularity in the volvocine green algae. Okasha’s concepts are a provocative step towards a more general understanding of the major (...) evolutionary transitions; however, the application of certain ideas to the volvocine model system is not straightforward. (shrink)

Adaptations can occur at different hierarchical levels, but it can be difficult to identify the level of adaptation in specific cases. A major problem is that selection at a lower level can filter up, creating the illusion of selection at a higher level. We use optimality modeling of the volvocine algae to explore the emergence of genuine group adaptations. We find that it is helpful to develop an explicit model for what group fitness would be in the absence of group-level (...) relationships between traits and group fitness. We call this “counterfactual fitness,” because in many actual cases of interest there are group-level relationships. Once counterfactual fitness is modeled, the difference between effects that filter up and genuine group selection is explicit and so, therefore, is the distinction between apparent and genuine group adaptations. We call the latter group-specific adaptations. Recognizing group-specific adaptations is important because only group-specific adaptations would cause the lower-level units to be maladapted if they were to leave the group and enter a global cell-level population. Thus, as group-specific adaptations evolve, they create selective pressure for increased cohesiveness and individuality of groups. This article suggests that group-specific adaptations could be present in the simplest, earliest branching colonial volvocine species, which do not have distinct specialized cells. The article also makes predictions about the kind of empirical evidence needed to support or refute the hypothesis that a particular trait is a group-level adaptation. (shrink)

Attempts to explain the origin of macroevolutionary innovations have been only partially successful. Here it is proposed that the patterns of major evolutionary transitions have to be understood first, before it is possible to further analyse the forces behind the process. The hypothesis is that major evolutionary innovations are characterized by an increase in organismal autonomy, in the sense of emancipation from the environment. After a brief overview of the literature on this subject, increasing autonomy is defined as the evolutionary (...) shift in the individual system–environment relationship, such that the direct influences of the environment are gradually reduced and a stabilization of self-referential, intrinsic functions within the system is generated. This is described as relative autonomy because numerous interconnections with the environment and dependencies upon it are retained. Features of increasing autonomy are spatial separations, an increase in homeostatic functions and in body size, internalizations and an increase in physiological and behavioral flexibility. It is described how these features are present in different combinations in the major evolutionary transitions of metazoans and, consequently, how they should be taken into consideration when evolutionary innovations are studied. The hypothesis contributes to a reconsideration of the relationship between organisms and their environment. (shrink)

Biologists have long theorized about the evolution of life cycles, meiosis, and sexual reproduction. We revisit these topics and propose that the fundamental difference between life cycles is where and when multicellularity is expressed. We develop a scenario to explain the evolutionary transition from the life cycle of a unicellular organism to one in which multicellularity is expressed in either the haploid or diploid phase, or both. We propose further that meiosis might have evolved as a mechanism to correct for (...) spontaneous whole‐genome duplication (auto‐polyploidy) and thus before the evolution of sexual reproduction sensu stricto (i.e. the formation of a diploid zygote via the fusion of haploid gametes) in the major eukaryotic clades. In addition, we propose, as others have, that sexual reproduction, which predominates in all eukaryotic clades, has many different advantages among which is that it produces variability among offspring and thus reduces sibling competition. (shrink)

Affective disorders arise in stressful situations from aberrant sensory information integration that affects energetic nutrient (i.e., glucose) utilization to the cognitive centers of the brain. Because energy flow is mediated by molecular signals and receptors that evolved before the first complex brains, the phylogenetically oldest signaling systems are essential in the etiology of affective disorders. The corticotropin‐releasing factor (CRF) peptide subfamily is a phylogenetically old metazoan peptide family and is pivotal for regulating organismal energy response associated with stress. Highly conserved, (...) both the CRF peptide family and its receptors possess a structural relationship to the teneurins, and their receptors, latrophilins, respectively. The CRF homologous region of teneurin is defined as the “teneurin C‐terminal associated peptide” (TCAP) and antagonizes CRF action, regulates mitochondrial energy production, and is anxiolytic in vivo. Here, it is postulated that TCAP represents an ancient peptide that mediates intercellular information transfer of stressful and noxious events by regulating energy utilization among neurons. (shrink)

Development is a process whereby a relatively unspecified system comprised of loosely connected lower level parts becomes organized into a coherent, higher-level agency. Its temporal corollaries are growth, increasingly deterministic behavior, and a progressive reduction of developmental potential. During immature stages with relatively low specification and high potential, development is largely controlled by local interactions from the “bottom-up,” whereas during more highly specified stages with reduced potential, emergent autocatalytic processes exert “top-down” control. Robert Ulanowicz has shown that this phenomenology of (...) ascendency follows thermodynamic principles and can be described quantitatively using information theory, providing a general theory of development. However, the theory has not found a wide audience among developmental biologists, as genetic determinism encourages the popular reductionistic perception that ontogeny is controlled entirely by molecular mechanisms that exert efficient causality from the bottom-up. Nonetheless, measurements of metabolic rates and mRNA complexity in developing embryos, as well as functional analyses of gene regulatory systems, indicate that ontogeny fits the paradigm of developmental ascendency. Beyond informing biomedical research and the interpretation of large datasets obtained by systems-biological approaches, developmental ascendency helps explain the origin of life, and, being independent of scale, provides an overarching explanation for phylogenetic change that contextualizes Darwinian evolution. (shrink)

All disciplines must define their basic units and core processes. In evolutionary biology, the core process is natural selection and the basic unit of selection and adaptation is the individual. To operationalize the theory of natural selection we must count individuals, as they are the bearers of fitness. While canonical individuals have often been taken to be multicellular organisms, the hierarchy of life shows that new kinds of individuals have evolved. A variety of criteria have been used to define biological (...) individuality. Some criteria rely on the presence/absence of a particular property while others advocate an approach that reflects the process of natural selection. The plethora of approaches to classifying individuality has resulted in confusion regarding how to study individuality in a given taxon. (shrink)

In this contribution, I comment on Raffaella Campaner’s defense of explanatory pluralism in psychiatry (in this volume). In her paper, Campaner focuses primarily on explanatory pluralism in contrast to explanatory reductionism. Furthermore, she distinguishes between pluralists who consider pluralism to be a temporary state on the one hand and pluralists who consider it to be a persisting state on the other hand. I suggest that it would be helpful to distinguish more than those two versions of pluralism – different understandings (...) of explanatory pluralism both within philosophy of science and psychiatry – namely moderate/temporary pluralism, anything goes pluralism, isolationist pluralism, integrative pluralism and interactive pluralism. Next, I discuss the pros and cons of these different understandings of explanatory pluralism. Finally, I raise the question of how to implement or operationalize explanatory pluralism in scientific practice; how to structure the “genuine dialogue” or shape “the pluralistic attitude” Campaner is referring to. As tentative answers, I explore a question-based framework for explanatory pluralism as well as social-epistemological procedures for interaction among competing approaches and explanations. (shrink)

The aim of this paper is to provide a theoretical framework to understand how multicellular systems realize functionally integrated physiological entities by organizing their intercellular space. From a perspective centered on physiology and integration, biological systems are often characterized as organized in such a way that they realize metabolic self-production and self-maintenance. The existence and activity of their components rely on the network they realize and on the continuous management of the exchange of matter and energy with their environment. One (...) of the virtues of the organismic approach focused on organization is that it can provide an understanding of how biological systems are functionally integrated into coherent wholes. Organismic frameworks have been primarily developed by focusing on unicellular life. Multicellularity, however, presents additional challenges to our understanding of biological systems, related to how cells are capable to live together in higher-order entities, in such a way that some of their features and behaviors are constrained and controlled by the system they realize. Whereas most accounts of multicellularity focus on cell differentiation and increase in size as the main elements to understand biological systems at this level of organization, we argue that these factors are insufficient to provide an understanding of how cells are physically and functionally integrated in a coherent system. In this paper, we provide a new theoretical framework to understand multicellularity, capable to overcome these issues. Our thesis is that one of the fundamental theoretical principles to understand multicellularity, which is missing or underdeveloped in current accounts, is the functional organization of the intercellular space. In our view, the capability to be organized in space plays a central role in this context, as it enables (and allows to exploit all the implications of) cell differentiation and increase in size, and even specialized functions such as immunity. We argue that the extracellular matrix plays a crucial active role in this respect, as an evolutionary ancient and specific (non-cellular) control subsystem that contributes as a key actor to the functional specification of the multicellular space and to modulate cell fate and behavior. We also analyze how multicellular systems exert control upon internal movement and communication. Finally, we show how the organization of space is involved in some of the failures of multicellular organization, such as aging and cancer. (shrink)