• Volume 39, Issue 2

April 2014,   pages  171-332

• Introduction: E Pluribus Unum

• Group behaviour in physical, chemical and biological systems

Groups exhibit properties that either are not perceived to exist, or perhaps cannot exist, at the individual level. Such emergent’ properties depend on how individuals interact, both among themselves and with their surroundings. The world of everyday objects consists of material entities. These are, ultimately, groups of elementary particles that organize themselves into atoms and molecules, occupy space, and so on. It turns out that an explanation of even the most commonplace features of this world requires relativistic quantum field theory and the fact that Planck’s constant is discrete, not zero. Groups of molecules in solution, in particular polymers (sols’), can form viscous clusters that behave like elastic solids (gels’). Sol-gel transitions are examples of cooperative phenomena. Their occurrence is explained by modelling the statistics of inter-unit interactions: the likelihood of either state varies sharply as a critical parameter crosses a threshold value. Group behaviour among cells or organisms is often heritable and therefore can evolve. This permits an additional, typically biological, explanation for it in terms of reproductive advantage, whether of the individual or of the group. There is no general agreement on the appropriate explanatory framework for understanding group-level phenomena in biology.

• Evolution, epigenetics and cooperation

Explanations for biological evolution in terms of changes in gene frequencies refer to outcomes rather than process. Integrating epigenetic studies with older evolutionary theories has drawn attention to the ways in which evolution occurs. Adaptation at the level of the gene is givingway to adaptation at the level of the organism and higher-order assemblages of organisms. These ideas impact on the theories of how cooperation might have evolved. Two of the theories, i.e. that cooperating individuals are genetically related or that they cooperate for self-interested reasons, have been accepted for a long time. The idea that adaptation takes place at the level of groups is much more controversial. However, bringing together studies of development with those of evolution is taking away much of the heat in the debate about the evolution of group behaviour.

• Symbiosis as the way of eukaryotic life: The dependent co-origination of the body

Molecular analyses of symbiotic relationships are challenging our biological definitions of individuality and supplanting them with a new notion of normal part–whole relationships. This new notion is that of a holobiont’, a consortium of organisms that becomes a functionally integrated whole’. This holobiont includes the zoological organism (the animal’) as well as its persistent microbial symbionts. This new individuality is seen on anatomical and physiological levels, where a diversity of symbionts form a new organ system’ within the zoological organism and become integrated into its metabolism and development. Moreover, as in normal development, there are reciprocal interactions between the host’ organism and its symbionts that alter gene expression in both sets of cells. The immune system, instead of being seen as functioning solely to keep microbes out of the body, is also found to develop, in part, in dialogue with symbionts. Moreover, the immune system is actively involved in the colonization of the zoological organism, functioning as a mechanism for integrating microbes into the animal-cell community. Symbionts have also been found to constitute a second mode of genetic inheritance, providing selectable genetic variation for natural selection. We develop, grow and evolve as multi-genomic consortia/teams/ecosystems.

• Limb, tooth, beak: Three modes of development and evolutionary innovation of form

The standard model of evolutionary change of form, deriving from Darwin’s theory via the Modern Synthesis, assumes a gradualistic reshaping of anatomical structures, with major changes only occurring by many cycles of natural selection for marginal adaptive advantage. This model, with its assertion that a single mechanism underlies both micro- and macroevolutionary change, contains an implicit notion of development which is only applicable in some cases. Here we compare the embryological processes that shape the vertebrate limb bud, the mammalian tooth and the avian beak. The implied notion of development in the standard evolutionary picture is met only in the case of the vertebrate limb, a single-primordium organ with morphostatic shaping, in which cells rearrange in response to signalling centres which are essentially unchanged by cell movement. In the case of the tooth, a single-primordium organ with morphodynamic shaping in which the strengths and relationships between signalling centres is influenced by the cell and tissue movements they induce, and the beak, in which the final form is influenced by the collision and rearrangement of multiple tissue primordia, abrupt appearance of qualitatively different forms (i.e. morphological novelties) can occur with small changes in system parameters induced by a genetic change, or by an environmental factor whose effects can be subsequently canalized genetically. Bringing developmental mechanisms and, specifically, the material properties of tissues as excitable media into the evolutionary picture, demonstrates that gradualistic change for incremental adaptive advantage is only one of the possible modes of morphological evolution.

• Sociobiology of the budding yeast

Social theory has provided a useful framework for research with microorganisms. Here I describe the advantages and possible risks of using a well-known model organism, the unicellular yeast Saccharomyces cerevisiae, for sociobiological research. I discuss the problems connected with clear classification of yeast behaviour based on the fitness-based Hamilton paradigm. Relevant traits include different types of communities, production of flocculins, invertase and toxins, and the presence of apoptosis.

• Nascent multicellular life and the emergence of individuality

The evolution of multicellular organisms from unicellular ancestors involves a shift in the level at which selection operates. It is usual to think about this shift in terms of the emergence of traits that cause heritable differences in reproductive output at the level of nascent collectives. Defining these traits and the causes of their origin lies at the heart of understanding the evolution of multicellular life. In working toward a mechanistic, take-nothing-for-granted account, we begin by recognizing that the standard Lewontin formulation of properties necessary and sufficient for evolution by natural selection does not necessarily encompass Darwinian evolution in primitive collectives where parent-offspring relationships may have been poorly defined. This, we suggest, limits the ability to conceptualize and capture the earliest manifestations of Darwinian properties. By way of solution we propose a relaxed interpretation of Lewontin’s conditions and present these in the form of a set of necessary requirements for evolution by natural selection based upon the establishment of genealogical connections between recurrences of collectives. With emphasis on genealogy – as opposed to reproduction – it is possible to conceive selection acting on collectives prior to any manifestation of heritable variance in fitness. Such possibility draws attention to the evolutionary emergence of traits that strengthen causal relationships between recurrences – traits likely to underpin the emergence of forms of multiplication that establish parent-offspring relationships. Application of this framework to collectives of marginal status, particularly those whose recurrence is not defined by genealogy, makes clear that change at the level of collectives need not arise from selection acting at the higher level. We conclude by outlining applicability of our framework to loosely defined collectives of cells, such as those comprising the slugs of social amoeba and microbes that constitute the human microbiome.

• The remarkable discreteness of being

Life is a discrete, stochastic phenomenon: for a biological organism, the time of the two most important events of its life (reproduction and death) is random and these events change the number of individuals of the species by single units. These facts can have surprising, counterintuitive consequences. I review here three examples where these facts play, or could play, important roles: the spatial distribution of species, the structuring of biodiversity and the (Darwinian) evolution of altruistic behaviour.

• An ensemble approach to the evolution of complex systems

Adaptive systems frequently incorporate complex structures which can arise spontaneously and which may be non-adaptive in the evolutionary sense. We give examples from phase transition and fractal growth to develop the themes of cooperative phenomena and pattern formation. We discuss RNA interference and transcriptional gene regulation networks, where a major part of the topological properties can be accounted for by mere combinatorics. A discussion of ensemble approaches to biological systems and measures of complexity is presented, and a connection is established between complexity and fitness.

• Competing views on cancer

Despite intense research efforts that have provided enormous insight, cancer continues to be a poorly understood disease. There has been much debate over whether the cancerous state can be said to originate in a single cell or whether it is a reflection of aberrant behaviour on the part of a ‘society of cells’. This article presents, in the form of a debate conducted among the authors, three views of how the problem might be addressed. We do not claim that the views exhaust all possibilities. These views are

• the tissue organization field theory (TOFT) that is based on a breakdown of tissue organization involving many cells from different embryological layers,
• the cancer stem cell (CSC) hypothesis that focuses on genetic and epigenetic changes that take place within single cells, and
• the proposition that rewiring of the cell’s protein interaction networks mediated by intrinsically disordered proteins (IDPs) drives the tumorigenic process.

The views are based on different philosophical approaches. In detail, they differ on some points and agree on others. It is left to the reader to decide whether one approach to understanding cancer appears more promising than the other.

• Origins of evolutionary transitions

An evolutionary transition in individuality’ or major transition’ is a transformation in the hierarchical level at which natural selection operates on a population. In this article I give an abstract (i.e. level-neutral and substrate-neutral) articulation of the transition process in order to precisely understand how such processes can happen, especially how they can get started.

• Individuals and groups in evolution: Darwinian pluralism and the multilevel selection debate

Outlined here is an updated review of the long-standing kin selection vs group selection’ debate. Group selection is a highly contentious concept, scientifically and philosophically. In 2012, Dawkins’ attack against Wilson’s latest book about eusociality concentrated all the attention on group selection and its mutual exclusivity with respect to inclusive fitness theory. Both opponents seem to be wrong, facing the general consensus in the field, which favours a pluralistic approach. Historically, despite some misunderstandings in current literature, such a perspective is clearly rooted in Darwin’s writings, which suggested a plurality of levels of selection and a general view that we propose to call imperfect selfishness’. Today, the mathematically updated hypothesis of group selection has little to do with earlier versions of group selection’. It does not imply ontologically unmanageable notions of groups’. We propose here population structure as the main criterion of compatibility between kin selection and group selection. The latter is now evidently a pattern among others within a more general `multilevel selection’ theory. Different explanations and patterns are not mutually exclusive. Such a Darwinian pluralism is not a piece of the past, but a path into the future. A challenge in philosophy of biology will be to figure out the logical structure of this emerging pluralistic theory of evolution in such contentious debates.

• A personal perspective on individual and group: Comparative cultural observations with a focus on Ibn Khaldun

As the Islamic world declined in the 14th century, Ibn Khaldun wrote the Muqaddimah, a massive philosophical work in which he sought scientific grounds for a universal analysis of human beings. By seeking a global history of humanity, one that was not derived from the particular history of any one group, he was able to offer insight into the importance of group solidarity, assabiyeh. In this essay, I discuss the dynamics between autonomous individuality and group identity and offer some cultural comparisons to illustrate more general insights.

• # Journal of Biosciences

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