The applicability of computational and dynamical systems models to organisms is scrutinized, using examples from developmental biology and cognition. Developmental morphogenesis is dependent on the ...inherent material properties of developing animal (metazoan) tissues, a non-computational modality, but cell differentiation, which utilizes chromatin-based revisable memory banks and program-like function-calling, via the developmental gene co-expression system unique to the metazoans, has a quasi-computational basis. Multi-attractor dynamical models are argued to be misapplied to global properties of development, and it is suggested that along with computationalism, classic forms of dynamicism are similarly unsuitable to accounting for cognitive phenomena. Proposals are made for treating brains and other nervous tissues as novel forms of excitable matter with inherent properties which enable the intensification of cell-based basal cognition capabilities present throughout the tree of life. Finally, some connections are drawn between the viewpoint described here and active inference models of cognition, such as the Free Energy Principle.
•Computational models of embryonic development are no longer tenable.•A material-inherency perspective is a better-supported alternative for morphogenesis.•Cell differentiation is based on quasi-computational capacities of metazoan cells.•Cognition studies can benefit from conceptual advances in developmental biology.
Abstract
Although discussed by 20th century philosophers in terms drawn from the sciences of non-living systems, in recent decades biological function has been considered in relationship to ...organismal capability and purpose. Bringing two phenomena generally neglected in evolutionary theory (i.e. inherency and agency) to bear on questions of function leads to a rejection of the adaptationist ‘selected effects’ notion of biological function. I review work showing that organisms such as the placozoans can thrive with almost no functional embellishments beyond those of their constituent cells and physical properties of their simple tissues. I also discuss work showing that individual tissue cells and their artificial aggregates exhibit agential behaviours that are unprecedented in the histories of their respective lineages. I review findings on the unique metazoan mechanism of developmental gene expression that has recruited, during evolution, inherent ancestral cellular functionalities into specialized cell types and organs of the different animal groups. I conclude that most essential functions in animal species are inherent to the cells from which they evolved, not selected effects, and that many of the others are optional ‘add-ons’, a status inimical to fitness-based models of evolution positing that traits emerge from stringent cycles of selection to meet external challenges.
•Cell differentiation has been modeled as dynamical or modular.•Current models draw on both approaches but neglect metazoan-specific gene regulation.•Condensed-phase nuclear hubs can exaggerate ...ancestral gene activities.•Enhancers and other regulatory novelties generate cell types from inherent functions.•Recruitment of Grainyhead for epithelium exemplifies evolution of differentiation.
I revisit two theories of cell differentiation in multicellular organisms published a half-century ago, Stuart Kauffman's global genome regulatory dynamics (GGRD) model and Roy Britten's and Eric Davidson's modular gene regulatory network (MGRN) model, in light of newer knowledge of mechanisms of gene regulation in the metazoans (animals). The two models continue to inform hypotheses and computational studies of differentiation of lineage-adjacent cell types. However, their shared notion (based on bacterial regulatory systems) of gene switches and networks built from them have constrained progress in understanding the dynamics and evolution of differentiation. Recent work has described unique write-read-rewrite chromatin-based expression encoding in eukaryotes, as well metazoan-specific processes of gene activation and silencing in condensed-phase, enhancer-recruiting regulatory hubs, employing disordered proteins, including transcription factors, with context-dependent identities. These findings suggest an evolutionary scenario in which the origination of differentiation in animals, rather than depending exclusively on adaptive natural selection, emerged as a consequence of a type of multicellularity in which the novel metazoan gene regulatory apparatus was readily mobilized to amplify and exaggerate inherent cell functions of unicellular ancestors. The plausibility of this hypothesis is illustrated by the evolution of the developmental role of Grainyhead-like in the formation of epithelium.
During development cells and tissues undergo changes in pattern and form that employ a wider range of physical mechanisms than at any other time in an organism's life. This book shows how physics can ...be used to analyze these biological phenomena. Written to be accessible to both biologists and physicists, major stages and components of the biological development process are introduced and then analyzed from the viewpoint of physics. The presentation of physical models requires no mathematics beyond basic calculus. Physical concepts introduced include diffusion, viscosity and elasticity, adhesion, dynamical systems, electrical potential, percolation, fractals, reaction-diffusion systems, and cellular automata. With full-color figures throughout, this comprehensive textbook teaches biophysics by application to developmental biology and is suitable for graduate and upper-undergraduate courses in physics and biology.
Using three examples drawn from animal systems, I advance the hypothesis that major transitions in multicellular evolution often involved the constitution of new cell-based materials with ...unprecedented morphogenetic capabilities. I term the materials and formative processes that arise when highly evolved cells are incorporated into mesoscale matter ‘biogeneric’, to reflect their commonality with, and distinctiveness from, the organizational properties of non-living materials. The first transition arose by the innovation of classical cell-adhesive cadherins with transmembrane linkage to the cytoskeleton and the appearance of the morphogen Wnt, transforming some ancestral unicellular holozoans into ‘liquid tissues’, and thereby originating the metazoans. The second transition involved the new capabilities, within a basal metazoan population, of producing a mechanically stable basal lamina, and of planar cell polarization. This gave rise to the eumetazoans, initially diploblastic (two-layered) forms, and then with the addition of extracellular matrices promoting epithelial–mesenchymal transformation, three-layered triploblasts. The last example is the fin-to-limb transition. Here, the components of a molecular network that promoted the development of species-idiosyncratic endoskeletal elements in gnathostome ancestors are proposed to have evolved to a dynamical regime in which they constituted a Turing-type reaction–diffusion system capable of organizing the stereotypical arrays of elements of lobe-finned fish and tetrapods. The contrasting implications of the biogeneric materials-based and neo-Darwinian perspectives for understanding major evolutionary transitions are discussed.
This article is part of the themed issue ‘The major synthetic evolutionary transitions’.
I discuss recent work on the origins of morphology and cell-type diversification in Metazoa - collectively the animals - and propose a scenario for how these two properties became integrated, with ...the help of a third set of processes, cellular pattern formation, into the developmental programs seen in present-day metazoans. Inherent propensities to generate familiar forms and cell types, in essence a parts kit for the animals, are exhibited by present-day organisms and were likely more prominent in primitive ones. The structural motifs of animal bodies and organs, e.g., multilayered, hollow, elongated and segmented tissues, internal and external appendages, branched tubes, and modular endoskeletons, can be accounted for by the properties of mesoscale masses of metazoan cells. These material properties, in turn, resulted from the recruitment of "generic" physical forces and mechanisms - adhesion, contraction, polarity, chemical oscillation, diffusion - by toolkit molecules that were partly conserved from unicellular holozoan antecedents and partly novel, distributed in the different metazoan phyla in a fashion correlated with morphological complexity. The specialized functions of the terminally differentiated cell types in animals, e.g., contraction, excitability, barrier function, detoxification, excretion, were already present in ancestral unicellular organisms. These functions were implemented in metazoan differentiation in some cases using the same transcription factors as in single-celled ancestors, although controlled by regulatory mechanisms that were hybrids between earlier-evolved processes and regulatory innovations, such as enhancers. Cellular pattern formation, mediated by released morphogens interacting with biochemically responsive and excitable tissues, drew on inherent self-organizing processes in proto-metazoans to transform clusters of holozoan cells into animal embryos and organs.
Organismal development occurs when expression of certain genes leads to the mobilization of physical forces and effects that shape and pattern multicellular clusters. All materials exhibit preferred ...forms, but the inherent morphological motifs of some, such as liquids and crystalline solids are well-characterized. Recent work has shown that the origin of the animals (Metazoa) was accompanied by the acquisition by their developing tissues of liquid-like and liquid-crystalline properties. This and the novel capacity to produce stiff internal substrata (basal laminae) set these organisms apart from their closest relatives by the propensity (predictable from their material nature) to form complex bodies and organs. Once functional forms became established, however, they were susceptible to further genetic change as well as partial or full supplanting of original physical determinants by different ones. This results in the increasingly recognized phenomenon of homomorphy, the presence of the same structure in descendent organisms, brought about by transformed developmental mechanisms.
Animal bodies and the embryos that generate them exhibit an assortment of stereotypie morphological motifs that first appeared more than half a billion years ago. During development cells arrange ...themselves into tissues with interior cavities and multiple layers with immiscible boundaries, containing patterned arrangements of cell types. These tissues go on to elongate, fold, segment, and form appendages. Their motifs are similar to the outcomes of physical processes generic to condensed, chemically excitable, viscoelastic materials, although the embryonic mechanisms that generate them are typically much more complex. I propose that the origins of animal development lay in the mobilization of physical organizational effects that resulted when certain gene products of single-celled ancestors came to operate on the spatial scale of multicellular aggregates.
Abstract
The multiple origins of multicellularity had far-reaching consequences ranging from the appearance of phenotypically complex life-forms to their effects on Earth’s aquatic and terrestrial ...ecosystems. Yet, many important questions remain. For example, do all lineages and clades share an ancestral developmental predisposition for multicellularity emerging from genomic and biophysical motifs shared from a last common ancestor, or are the multiple origins of multicellularity truly independent evolutionary events? In this review, we highlight recent developments and pitfalls in understanding the evolution of multicellularity with an emphasis on plants (here defined broadly to include the polyphyletic algae), but also draw upon insights from animals and their holozoan relatives, fungi and amoebozoans. Based on our review, we conclude that the evolution of multicellular organisms requires three phases (origination by disparate cell–cell attachment modalities, followed by integration by lineage-specific physiological mechanisms, and autonomization by natural selection) that have been achieved differently in different lineages.
The evolution of multicellular organisms, which requires three phases (origination, integration, and autonomization), has been achieved differently in different lineages.
SUMMARY
Multicellularity has evolved in several eukaryotic lineages leading to plants, fungi, and animals. Theoretically, in each case, this involved (1) cell‐to‐cell adhesion with an ...alignment‐of‐fitness among cells, (2) cell‐to‐cell communication, cooperation, and specialization with an export‐of‐fitness to a multicellular organism, and (3) in some cases, a transition from “simple” to “complex” multicellularity. When mapped onto a matrix of morphologies based on developmental and physical rules for plants, these three phases help to identify a “unicellular ⇒ colonial ⇒ filamentous (unbranched ⇒ branched) ⇒ pseudoparenchymatous ⇒ parenchymatous” morphological transformation series that is consistent with trends observed within each of the three major plant clades. In contrast, a more direct “unicellular ⇒ colonial or siphonous ⇒ parenchymatous” series is observed in fungal and animal lineages. In these contexts, we discuss the roles played by the cooptation, expansion, and subsequent diversification of ancestral genomic toolkits and patterning modules during the evolution of multicellularity. We conclude that the extent to which multicellularity is achieved using the same toolkits and modules (and thus the extent to which multicellularity is homologous among different organisms) differs among clades and even among some closely related lineages.
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