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Self-Organization at Different Levels of Metazoan Complexity in Comparative Genomic–Phenomic Context
Abstract
The chapter presents an analytic description of evolutionary and developmental morphogenetic events in Metazoa using concepts of self-organization, morphological and molecular–genetic data, and the topological approach to the analysis. Biological objects are complex systems capable of dynamic self-organization at all levels of biological complexity. Some examples of self-organization in cyanobacteria, metazoan cells in vitro (chick embryo myogenic cells, molluscan hemocytes, sea urchin embryo cells), and animal communities of some vertebrates are shown. Following René Thom, a topological interpretation of some evolutionary and developmental transformations is presented using well-known mathematical concepts. Toroidal forms are considered as examples of functionally optimized biological design and attractors in metazoan morphogenesis. Molecular–genetic evidence of genomic–phenomic correlations determining the body plan and evolutionary trajectories in Metazoa is discussed. Gene regulatory networks and whole metazoan genomes are interpreted as self-organizing network systems dynamically transforming in development and evolution. Symmetry breaking, topological discontinuities and catastrophes, and body plan transformations are fundamental phenomena in metazoan development and evolution.
... Evolutionary biology is one of the main areas where complexity theory has been used in order to gain a better understanding of the processes of evolution and adaptation. It appears that there is a link between cooperation and the self-organization of dissipative structures, at least as far as organisms are concerned [12]. In that sense, cooperation could be seen as an emergent property of biological systems, leading to self-organization. ...
Cooperation is a pillar not only of human societies but also of evolution. The most important cooperation mechanisms, which are not based on kinship, are indirect reciprocity and spatialselection. They influence the distribution of genes among a population but could also play a role in developmental biology by distributing inductive factors within the initial cell population. The paper examines the relationship between cooperative mechanisms deployed by biological organisms and the principles and theory of distributive justice, which is the legal foundation of cooperation.
Keywords: Cooperation; indirect reciprocity; spatial selection; distributive justice
We investigate the emergence of global alignment in colonies of dividing rod-shaped cells under confinement. Using molecular dynamics simulations and continuous modeling, we demonstrate that geometrical anisotropies in the confining environment give rise to an imbalance in the normal stresses, which, in turn, drives a collective rearrangement of the cells. This behavior crucially relies on the colony’s solid-like mechanical response at short time scales and can be recovered within the framework of active hydrodynamics upon modeling bacterial colonies as growing viscoelastic gels characterized by Maxwell-like stress relaxation.
In this review, we consider transformations of axial symmetry in metazoan evolution and development, the genetic basis, and phenotypic expressions of different axial body plans. In addition to the main symmetry types in metazoan body plans, such as rotation (radial symmetry), reflection (mirror and glide reflection symmetry), and translation (metamerism), many biological objects show scale (fractal) symmetry as well as some symmetry-type combinations. Some genetic mechanisms of axial pattern establishment, creating a coordinate system of a metazoan body plan, bilaterian segmentation, and left–right symmetry/asymmetry, are analysed. Data on the crucial contribution of coupled functions of the Wnt, BMP, Notch, and Hedgehog signaling pathways (all pathways are designated according to the abbreviated or full names of genes or their protein products; for details, see below) and the axial Hox-code in the formation and maintenance of metazoan body plans are necessary for an understanding of the evolutionary diversification and phenotypic expression of various types of axial symmetry. The lost body plans of some extinct Ediacaran and early Cambrian metazoans are also considered in comparison with axial body plans and posterior growth in living animals.
Self-organization can be broadly defined as the ability of a system to display ordered spatiotemporal patterns solely as the result of the interactions among the system components. Processes of this kind characterize both living and artificial systems, making self-organization a concept that is at the basis of several disciplines, from physics to biology and engineering. Placed at the frontiers between disciplines, artificial life (ALife) has heavily borrowed concepts and tools from the study of self-organization, providing mechanistic interpretations of lifelike phenomena as well as useful constructivist approaches to artificial system design. Despite its broad usage within ALife, the concept of self-organization has been often excessively stretched or misinterpreted, calling for a clarification that could help with tracing the borders between what can and cannot be considered self-organization. In this review, we discuss the fundamental aspects of self-organization and list the main usages within three primary ALife domains, namely “soft” (mathematical/computational modeling), “hard” (physical robots), and “wet” (chemical/biological systems) ALife. We also provide a classification to locate this research. Finally, we discuss the usefulness of self-organization and related concepts within ALife studies, point to perspectives and challenges for future research, and list open questions. We hope that this work will motivate discussions related to self-organization in ALife and related fields.
Background:
The homeobox genes Pdx and Cdx are widespread across the animal kingdom and part of the small ParaHox gene cluster. Gene expression patterns suggest ancient roles for Pdx and Cdx in patterning the through-gut of bilaterian animals although functional data are available for few lineages. To examine evolutionary conservation of Pdx and Cdx gene functions, we focus on amphioxus, small marine animals that occupy a pivotal position in chordate evolution and in which ParaHox gene clustering was first reported.
Results:
Using transcription activator-like effector nucleases (TALENs), we engineer frameshift mutations in the Pdx and Cdx genes of the amphioxus Branchiostoma floridae and establish mutant lines. Homozygous Pdx mutants have a defect in amphioxus endoderm, manifest as loss of a midgut region expressing endogenous GFP. The anus fails to open in homozygous Cdx mutants, which also have defects in posterior body extension and epidermal tail fin development. Treatment with an inverse agonist of retinoic acid (RA) signalling partially rescues the axial and tail fin phenotypes indicating they are caused by increased RA signalling. Gene expression analyses and luciferase assays suggest that posterior RA levels are kept low in wild type animals by a likely direct transcriptional regulation of a Cyp26 gene by Cdx. Transcriptome analysis reveals extensive gene expression changes in mutants, with a disproportionate effect of Pdx and Cdx on gut-enriched genes and a colinear-like effect of Cdx on Hox genes.
Conclusions:
These data reveal that amphioxus Pdx and Cdx have roles in specifying middle and posterior cell fates in the endoderm of the gut, roles that likely date to the origin of Bilateria. This conclusion is consistent with these two ParaHox genes playing a role in the origin of the bilaterian through-gut with a distinct anus, morphological innovations that contributed to ecological change in the Cambrian. In addition, we find that amphioxus Cdx promotes body axis extension through a molecular mechanism conserved with vertebrates. The axial extension role for Cdx dates back at least to the origin of Chordata and may have facilitated the evolution of the post-anal tail and active locomotion in chordates.
Nutrient cycling is an emergent property of ecosystems at all scales, from microbial communities to the entire biosphere. Understanding how nutrient cycles emerge from the collective metabolism of ecosystems is a challenging problem. Here we use closed microbial ecosystems (CES), hermetically sealed consortia that sustain nutrient cycles when provided with only light, to learn how microbial communities cycle carbon. A new technique for quantifying carbon exchange shows that CES comprised of an alga and diverse bacteria self-organize to robustly cycle carbon. Comparing a library of CES, we find that carbon cycling does not depend strongly on the taxonomy of the bacteria present. Metabolic profiling reveals functional redundancy across CES: despite strong taxonomic differences, self-organized CES exhibit a conserved set of metabolic capabilities.
Summary
Closed microbial communities of algae and bacteria self-organize to robustly cycle carbon via emergent metabolite exchange.
Metazoan body plans combine well-defined primary, secondary, and in many bilaterians, tertiary body axes with structural asymmetries at multiple scales. Despite decades of study, how axis-defining symmetries and system-defining asymmetries co-emerge during both evolution and development remain open questions. Regeneration studies in asexual planaria have demonstrated an array of viable forms with symmetrized and, in some cases, duplicated body axes. We suggest that such forms may point toward an ancestral eumetazoan form with characteristics of both cnidarians and placazoa.
While the organization of inanimate systems such as gases or liquids is predominantly thermodynamically driven-a mixture of two gases will tend to mix until they reach equilibrium-biological systems frequently exhibit organization that is far from a well-mixed equilibrium. The anisotropies displayed by cells are evident in some of the dynamic processes that constitute life including cell development, movement, and division. These anisotropies operate at different length-scales, from the meso- to the nanoscale, and are proposed to reflect self-organization, a characteristic of living systems that is becoming accessible to reconstitution from purified components, and thus a more thorough understanding. Here, some examples of self-organization underlying cellular anisotropies at the cellular level are reviewed, with an emphasis on Rho-family GTPases operating at the plasma membrane. Given the technical challenges of studying these dynamic proteins, some of the successful approaches that are being employed to study their self-organization will also be considered.
Significance
Microorganisms can cooperate by secreting public goods that benefit local neighbors; however, the conditions that favor cooperative growth in the environment, and the way in which this growth alters microbes’ contribution to ecosystem functions, remain unexplored. Here, we show that cooperation mediates the degradation of polysaccharide particles recalcitrant to hydrolysis in aquatic environments. Combining experiments and models, we define the physiological and environmental parameters that mediate the transition from cooperation to competition. Cooperation emerges through the self-organization of cells into ∼10- to 20-µm clusters that enable uptake of diffusible hydrolysis products. When cooperation is required, the degradation of recalcitrant biopolymers can only take place when degraders exceed a critical cell concentration, underscoring the importance of microbial interactions for ecosystem function.
Posterior elongation of the developing embryo is a common feature of animal development. One group of genes that is involved in posterior elongation is represented by the Wnt genes, secreted glycoprotein ligands that signal to specific receptors on neighbouring cells and thereby establish cell-to-cell communication. In segmented animals such as annelids and arthropods, Wnt signalling is also likely involved in segment border formation and regionalisation of the segments. Priapulids represent unsegmented worms that are distantly related to arthropods. Despite their interesting phylogenetic position and their importance for the understanding of ecdysozoan evolution, priapulids still represent a highly underinvestigated group of animals. Here, we study the embryonic expression patterns of the complete sets of Wnt genes in the priapulids Priapulus caudatus and Halicryptus spinulosus. We find that both priapulids possess a complete set of 12 Wnt genes. At least in Priapulus, most of these genes are expressed in and around the posterior-located blastopore and thus likely play a role in posterior elongation. Together with previous work on the expression of other genetic factors such as caudal and even-skipped, this suggests that posterior elongation in priapulids is under control of the same (or very similar) conserved gene regulatory network as in arthropods.
The emergence of multiple axes is an essential element in the establishment of the mammalian body plan. This process takes place shortly after implantation of the embryo within the uterus and relies on the activity of gene regulatory networks that coordinate transcription in space and time. Whereas genetic approaches have revealed important aspects of these processes1, a mechanistic understanding is hampered by the poor experimental accessibility of early post-implantation stages. Here we show that small aggregates of mouse embryonic stem cells (ESCs), when stimulated to undergo gastrulation-like events and elongation in vitro, can organize a post-occipital pattern of neural, mesodermal and endodermal derivatives that mimic embryonic spatial and temporal gene expression. The establishment of the three major body axes in these 'gastruloids'2,3 suggests that the mechanisms involved are interdependent. Specifically, gastruloids display the hallmarks of axial gene regulatory systems as exemplified by the implementation of collinear Hox transcriptional patterns along an extending antero-posterior axis. These results reveal an unanticipated self-organizing capacity of aggregated ESCs and suggest that gastruloids could be used as a complementary system to study early developmental events in the mammalian embryo.
From microbial communities to cancer cells, many such complex collectives embody emergent and self-organising behaviour. Such behaviour drives cells to develop composite features such as formation of aggregates or expression of specific genes as a result of cell-cell interactions within a cell population. Currently, we lack universal mathematical tools for analysing the collective behaviour of biological swarms. To address this, we propose a multifractal inspired framework to measure the degree of emergence and self-organisation from scarce spatial (geometric) data and apply it to investigate the evolution of the spatial arrangement of Enterobacter cloacae aggregates. In a plate of semi-solid media, Enterobacter cloacae form a spatially extended pattern of high cell density aggregates. These aggregates nucleate from the site of inoculation and radiate outward to fill the entire plate. Multifractal analysis was used to characterise these patterns and calculate dynamics changes in emergence and self-organisation within the bacterial population. In particular, experimental results suggest that the new aggregates align their location with respect to the old ones leading to a decrease in emergence and increase in self-organisation.
Creating ordered structures from chaotic environments is at the core of biological processes at the subcellular, cellular and organismic level. In this perspective, we explore the physical as well as biological features of two prominent concepts driving self-organization, namely phase transition and reaction–diffusion, before closing with a discussion on open questions and future challenges associated with studying self-organizing systems.
This article is part of the theme issue ‘Self-organization in cell biology’.
Self-organization refers to the emergence of an overall order in time and space of a given system that results from the collective interactions of its individual components. This concept has been widely recognized as a core principle in pattern formation for multi-component systems of the physical, chemical and biological world. It can be distinguished from self-assembly by the constant input of energy required to maintain order—and self-organization therefore typically occurs in non-equilibrium or dissipative systems. Cells, with their constant energy consumption and myriads of local interactions between distinct proteins, lipids, carbohydrates and nucleic acids, represent the perfect playground for self-organization. It therefore comes as no surprise that many properties and features of self-organized systems, such as spontaneous formation of patterns, nonlinear coupling of reactions, bi-stable switches, waves and oscillations, are found in all aspects of modern cell biology. Ultimately, self-organization lies at the heart of the robustness and adaptability found in cellular and organismal organization, and hence constitutes a fundamental basis for natural selection and evolution.
This article is part of the theme issue ‘Self-organization in cell biology’.
Myosin II filaments form ordered superstructures in both cross-striated muscle and non-muscle cells. In cross-striated muscle, myosin II (thick) filaments, actin (thin) filaments and elastic titin filaments comprise the stereotypical contractile units of muscles called sarcomeres. Linear chains of sarcomeres, called myofibrils, are aligned laterally in registry to form cross-striated muscle cells. The experimentally observed dependence of the registered organization of myofibrils on extracellular matrix elasticity has been proposed to arise from the interactions of sarcomeric contractile elements (considered as force dipoles) through the matrix. Non-muscle cells form small bipolar filaments built of less than 30 myosin II molecules. These filaments are associated in registry forming superstructures (‘stacks’) orthogonal to actin filament bundles. Formation of myosin II filament stacks requires the myosin II ATPase activity and function of the actin filament crosslinking, polymerizing and depolymerizing proteins. We propose that the myosin II filaments embedded into elastic, intervening actin network (IVN) function as force dipoles that interact attractively through the IVN. This is in analogy with the theoretical picture developed for myofibrils where the elastic medium is now the actin cytoskeleton itself. Myosin stack formation in non-muscle cells provides a novel mechanism for the self-organization of the actin cytoskeleton at the level of the entire cell.
This article is part of the theme issue ‘Self-organization in cell biology’.
Significance
Embryonic development of any animal species is a robust series of morphogenetic events tightly controlled by molecular signals. However, the variety of developmental trajectories undertaken by different members of the same phylum suggests that normal development in each particular species might involve only a subset of morphogenetic capacities available to the highly developmentally plastic embryonic cells. Here we show that, faced by a new developmental context, the aggregates of dissociated gastrula cells of the sea anemone Nematostella vectensis use an alternative developmental trajectory typical for other, distantly related members of the cnidarian phylum. We conclude that new modes of development may evolve relatively easily due to the versatility and developmental plasticity of embryonic cells.
Rocks of the Ediacaran System (635-541 Ma) preserve fossil evidence of some of the earliest complex macroscopic organisms, many of which have been interpreted as animals. However, the unusual morphologies of some of these organisms have made it difficult to resolve their biological relationships to modern metazoan groups. Alternative competing phylogenetic interpretations have been proposed for Ediacaran taxa, including algae, fungi, lichens, rhizoid protists, and even an extinct higher-order group (Vendobionta). If a metazoan affinity can be demonstrated for these organisms, as advocated by many researchers, they could prove informative in debates concerning the evolution of the metazoan body axis, the making and breaking of axial symmetries, and the appearance of a metameric body plan. Attempts to decipher members of the enigmatic Ediacaran macrobiota have largely involved study of morphology: comparative analysis of their developmental phases has received little attention. Here we present what is known of ontogeny across the three iconic Ediacaran taxa Charnia masoni, Dickinsonia costata and Pteridinium simplex, together with new ontogenetic data and insights. We use these data and interpretations to re-evaluate the phylogenetic position of the broader Ediacaran morphogroups to which these taxa are considered to belong (rangeomorphs, dickinsoniomorphs and erniettomorphs). We conclude, based on the available evidence, that the affinities of the rangeomorphs and the dickinsoniomorphs lie within Metazoa.
Collinear regulation of Hox genes in space and time has been an outstanding question ever since the initial work of Ed Lewis in 1978. Here we discuss recent advances in our understanding of this phenomenon in relation to novel concepts associated with large-scale regulation and chromatin structure during the development of both axial and limb patterns. We further discuss how this sequential transcriptional activation marks embryonic stemcell-like axial progenitors in mammals and, consequently, how a temporal genetic system is further translated into spatial coordinates via the fate of these progenitors. In this context, we argue the benefit and necessity of implementing this unique mechanism as well as the difficulty in evolving an alternative strategy to deliver this critical positional information.
Cdx and Hox transcription factors are important regulators of axial patterning and are required for tissue generation along the vertebrate body axis. Cdx genes have been demonstrated to act upstream of Hox genes in midgestation embryos. Here, we investigate the role of Cdx transcription factors in the gradual colinear activation of the Hox clusters. We found that Hox temporally colinear expression is severely affected in epiblast stem cells derived from Cdx null embryos. We demonstrate that after initiation of 3′ Hox gene transcription, Cdx activity is crucial for H3K27ac deposition and for accessibility of cis-regulatory elements around the central – or 'trunk' – Hox genes. We thereby identify a Cdx-responsive segment of HoxA, immediately 5′ to the recently defined regulatory domain orchestrating initial transcription of the first Hox gene. We propose that this partition of HoxA into a Wnt-driven 3′ part and the newly found Cdx-dependent middle segment of the cluster, forms a structural fundament of Hox colinearity of expression. Subsequently to initial Wnt-induced activation of 3′ Hox genes, Cdx transcription factors would act as crucial effectors for activating central Hox genes, until the last gene of the cluster arrests the process.
Self-organization and natural selection are fundamental forces that shape the natural world. Substantial progress in understanding how these forces interact has been made through the study of abstract models. Further progress may be made by identifying a model system in which the interaction between self-organization and selection can be investigated empirically. To this end, we investigate how the self-organizing thermoregulatory huddling behaviours displayed by many species of mammals might influence natural selection of the genetic components of metabolism. By applying a simple evolutionary algorithm to a wellestablished model of the interactions between environmental, morphological, physiological and behavioural components of thermoregulation, we arrive at a clear, but counterintuitive, prediction: rodents that are able to huddle together in cold environments should evolve a lower thermal conductance at a faster rate than animals reared in isolation. The model therefore explains how evolution can be accelerated as a consequence of relaxed selection, and it predicts how the effect may be exaggerated by an increase in the litter size, i.e. by an increase in the capacity to use huddling behaviours for thermoregulation. Confirmation of these predictions in future experiments with rodents would constitute strong evidence of a mechanism by which self-organization can guide natural selection.
Metazoan evolution encompasses a vast evolutionary time scale spanning over 600 million years. Our ability to infer ancestral metazoan characters, both morphological and functional, is limited by our understanding of the nature and evolutionary dynamics of the underlying regulatory networks. Increasing coverage of metazoan genomes enables us to identify the evolutionary changes of the relevant genomic characters such as the loss or gain of coding sequences, gene duplications, micro- and macro-synteny, and non-coding element evolution in different lineages. In this review we describe recent advances in our understanding of ancestral metazoan coding and non-coding features, as deduced from genomic comparisons. Some genomic changes such as innovations in gene and linkage content occur at different rates across metazoan clades, suggesting some level of independence among genomic characters. While their contribution to biological innovation remains largely unclear, we review recent literature about certain genomic changes that do correlate with changes to specific developmental pathways and metazoan innovations. In particular, we discuss the origins of the recently described pharyngeal cluster which is conserved across deuterostome genomes, and highlight different genomic features that have contributed to the evolution of this group. We also assess our current capacity to infer ancestral metazoan states from gene models and comparative genomics tools and elaborate on the future directions of metazoan comparative genomics relevant to evo-devo studies.
Sequential 3 ′-to-5 ′ activation of the Hox gene clusters in early embryos is a most fascinating issue in developmental biology. Neither the trigger nor the regulatory elements involved in the transcriptional initiation of the 3 ′-most Hox genes have been unraveled in any organism. We demonstrate that a series of enhancers, some of which are Wnt-dependent, is located within a HoxA 3 ′ subtopologically associated domain (subTAD). This subTAD forms the structural basis for multiple layers of 3 ′-polarized features, including DNA accessibility and enhancer activation. Deletion of the cassette of Wnt-dependent enhancers proves its crucial role in initial transcription of HoxA at the 3 ′ side of the cluster.
The 21st century genomics-based analysis of evolutionary variation reveals a number of novel features impossible to predict when Dobzhansky and other evolutionary biologists formulated the neo-Darwinian Modern Synthesis in the middle of the last century. These include three distinct realms of cell evolution; symbiogenetic fusions forming eukaryotic cells with multiple genome compartments; horizontal organelle, virus and DNA transfers; functional organization of proteins as systems of interacting domains subject to rapid evolution by exon shuffling and exonization; distributed genome networks integrated by mobile repetitive regulatory signals; and regulation of multicellular development by non-coding lncRNAs containing repetitive sequence components. Rather than single gene traits, all phenotypes involve coordinated activity by multiple interacting cell molecules. Genomes contain abundant and functional repetitive components in addition to the unique coding sequences envisaged in the early days of molecular biology. Combinatorial coding, plus the biochemical abilities cells possess to rearrange DNA molecules, constitute a powerful toolbox for adaptive genome rewriting. That is, cells possess “Read–Write Genomes” they alter by numerous biochemical processes capable of rapidly restructuring cellular DNA molecules. Rather than viewing genome evolution as a series of accidental modifications, we can now study it as a complex biological process of active self-modification.
This review summarizes literature data on phylogenomics, indicating genomic–morphogenetic
correlations that determine the metazoan body plan and phenotypic complexity. Radical, macroevolutionary
transformations of the bilaterian body plan, which correlate with duplications or losses of individual Hox
genes of an ancestral cluster, or with its topological reorganization, are revealed. Regressive evolution is rather
common in Metazoa; reduction and simplification of the genome and phenome occurred quite often in the
evolution of metazoans. Since the system of cluster Hox genes has been shown to be the key regulatory node
of genome–phenome relationships, regulating a wide range of developmental processes, as well as being the
correlation node determining different evolutionary trajectories of various bilaterian taxa, it is a highly infor�mative correlate and indicator of evolutionary changes of the body plan.
Interconnected ensembles of biological entities are perhaps some of the most complex systems that modern science has encountered so far. In particular, scientists have concentrated on understanding how the complexity of the interacting structure between different neurons, proteins, or species influences the functioning of their respective systems. It is well established that many biological networks are constructed in a highly hierarchical way with two main properties: short average paths that join two apparently distant nodes (neuronal, species, or protein patches) and a high proportion of nodes in modular aggregations. Although several hypotheses have been proposed so far, still little is known about the relation of the modules with the dynamical activity in such biological systems. Here we show that network modularity is a key ingredient for the formation of self-organizing patterns of functional activity, independently of the topological peculiarities of the structure of the modules. In particular, we propose a self-organizing mechanism which explains the formation of macroscopic spatial patterns, which are homogeneous within modules. This may explain how spontaneous order in biological networks follows their modular structural organization. We test our results on real-world networks to confirm the important role of modularity in creating macroscale patterns.
Many fundamental cellular processes such as division, polarization, endocytosis, and motility require the assembly, maintenance, and disassembly of filamentous actin (F-actin) networks at specific locations and times within the cell. The particular function of each network is governed by F-actin organization, size, and density as well as by its dynamics. The distinct characteristics of different F-actin networks are determined through the coordinated actions of specific sets of actin-binding proteins (ABPs). Furthermore, a cell typically assembles and uses multiple F-actin networks simultaneously within a common cytoplasm, so these networks must self-organize from a common pool of shared globular actin (G-actin) monomers and overlapping sets of ABPs. Recent advances in multicolor imaging and analysis of ABPs and their associated F-actin networks in cells, as well as the development of sophisticated in vitro reconstitutions of networks with ensembles of ABPs, have allowed the field to start uncovering the underlying principles by which cells self-organize diverse F-actin networks to execute basic cellular functions.
The origins and the early evolution of multicellular animals required the exploitation of holozoan genomic regulatory elements and the acquisition of new regulatory tools. Comparative studies of metazoans and their relatives now allow reconstruction of the evolution of the metazoan regulatory genome, but the deep conservation of many genes has led to varied hypotheses about the morphology of early animals and the extent of developmental co-option. In this Review, I assess the emerging view that the early diversification of animals involved small organisms with diverse cell types, but largely lacking complex developmental patterning, which evolved independently in different bilaterian clades during the Cambrian Explosion.
Ecosystems are complex adaptive systems (CAS) by nature, which means that macroscopic patterns and properties emerge from, and feed back to affect, the interactions among adaptive individual ecological agents. These agents then further adapt (genetically) to the outcomes of those interactions. The concept of self-organization has become increasingly important for understanding ecosystem spatial heterogeneity and its consequences. It is well accepted that ecosystems can self-organize, and that resulting spatial structures carry functional consequences. Feedbacks from the outcome of spatial pattern to the individual agents from which patterns emerge, are an essential component of the definition of CAS but have been rarely examined for ecosystems. We explore whether spatial self-organization provides a mechanism for such feedback for ecosystems as CAS, that is, whether ecosystem-level outcomes of self-organized patterning could feed back to affect or even reinforce local pattern-forming processes at the agent level. Diffuse feedbacks of ecological and evolutionary significance ensue as a result of spatial heterogeneity and regular patterning, whether this spatial heterogeneity results from an underlying template effect or from self-organization. However, feedbacks directed specifically at pattern-forming agents to enhance pattern formation-reinforcing feedback-depend upon the level of organization of agents. Reinforcing evolutionary feedbacks occur at the individual level or below. At the ecosystem level, evidence for mechanisms of feedback from outcomes to patterning to agents forming the patterning remain tenuous. Spatial self-organization is a powerful dynamic in ecosystem and landscape science but feedbacks have been only loosely integrated so far. Self-organized patterns influencing dynamics at the ecosystem level represent "order for free". Whether or not this free order generated at the ecosystem level carries evolutionary function or is merely epiphenomenal is a fundamental question that we address here.
Comparative genomics helps to link characteristics of the genome and evolutionary trajectories by revealing the genomic correlates of morphological complexity and differences in the body plans of multicellular animals. Comparison of the organization of Hox clusters and expression of Hox genes with organismal morphology allows the emergence of macroevolutionary innovations as changes in morphogenesis and body plan of Bilateria, depending on the pattern of Hox code to be traced. We examine a correlation node that includes various types of organization of clustered (initially) Hox genes, early embryogenesis type, cellular developmental resources, thereby determining alternative evolutionary trajectories of various Bilateria taxa. Biological diversity inevitably manifests itself at all levels of organization and all stages of the evolution of the animal world, and therefore the reduction of the evolutionary strategies of Bilateria, and, moreover, all Metazoa, to a few simplified versions is impossible.
Stuart Kauffman here presents a brilliant new paradigm for evolutionary biology, one that extends the basic concepts of Darwinian evolution to accommodate recent findings and perspectives from the fields of biology, physics, chemistry and mathematics. The book drives to the heart of the exciting debate on the origins of life and maintenance of order in complex biological systems. It focuses on the concept of self-organization: the spontaneous emergence of order widely observed throughout nature. Kauffman here argues that self-organization plays an important role in the emergence of life itself and may play as fundamental a role in shaping life's subsequent evolution as does the Darwinian process of natural selection. Yet until now no systematic effort has been made to incorporate the concept of self-organization into evolutionary theory. The construction requirements which permit complex systems to adapt remain poorly understood, as is the extent to which selection itself can yield systems able to adapt more successfully. This book explores these themes. It shows how complex systems, contrary to expectations, can spontaneously exhibit stunning degrees of order, and how this order, in turn, is essential for understanding the emergence and development of life on Earth. Topics include the new biotechnology of applied molecular evolution, with its important implications for developing new drugs and vaccines; the balance between order and chaos observed in many naturally occurring systems; new insights concerning the predictive power of statistical mechanics in biology; and other major issues. Indeed, the approaches investigated here may prove to be the new center around which biological science itself will evolve. The work is written for all those interested in the cutting edge of research in the life sciences.
The structures of animal skeletons converge repeatedly on a limited number of architectural designs that can be constructed by growing organisms and that are functionally viable, although often not optimal. Properties of materials, construction rules that determine patterns of development, and physical constraints exerted by the requirements of function suggest that organic structure must necessarily approach these recurrent elements of design. A set of potential designs for the elements of animal skeletons is derived in terms of geometric and construction rules and the properties of materials. Skeletons of actual living and extinct organisms are matched with the possibilities defined within this theoretical morphospace. This provides a metric of skeletal complexity and of the extent to which various groups of animals have been able to exploit the range of possibilities of organic structure. These analyses show that the most evolutionarily advanced animals within a given phylum do not have the most complex skeletons; that arthropods are less morphologically diverse than vertebrates and molluscs; that the physical constraints of life on land and in the air substantially limit the variety of skeletal structures suitable for life in these environments; and that overall the range of possible skeletal designs has been very fully exploited by living and extinct organisms. These results strongly support the hypothesis that the essential elements of organic design are inherent in the material properties of the universe. The organizational properties of animal skeletons suggest that their design elements are fixed point attractors, structures that we characterize as topological attractors that evolution cannot avoid.
Cell movements during embryogenesis produce mechanical tensions that shape the embryo and can also regulate gene expression, thereby affecting cell differentiation. Increasing evidence indicates that mechano-sensitive regulation of gene expression plays important roles during embryogenesis by coupling the processes of morphogenesis and differentiation. However, the molecular mechanisms of this phenomenon remain poorly understood. This review focuses on the molecular mechanisms that "translate" mechanical stimuli into gene expression. This article is protected by copyright. All rights reserved.
Morphogenesis in living tissues is the paramount example of a time- and space-dependent orchestration of living matter where shape and order emerge from undifferentiated initial conditions. The genes encode the protein expression that eventually drives the emergence of the phenotype, while energy supply and cell-to-cell communication mechanisms are necessary to such a process. The overall control of the system likely exploits the laws of chemistry and physics through robust and universal processes. Even if the identification of the communication mechanisms is a question of fundamental nature, a long-standing investigation settled in the realm of chemical factors only (also known as morphogens) faces a number of apparently unsolvable questions. In this paper, we investigate at what extent mechanical forces, alone or through their biological feedbacks, can direct some basic aspects of morphogenesis in development biology. In this branch of mechano-biology, we discuss the typical rheological regimes of soft living matter and the related forces, providing a survey on how local mechanical feedbacks can control global size or even gene expression. We finally highlight the pivotal role of nonlinear mechanics to explain the emergence of complex shapes in living matter.
There were multiple prerequisites to the evolution of multicellular animal life, including the generation of multiple cell fates (“cellular diversity”) and their patterned spatial arrangement (“spatial form”). Wnt proteins operate as primordial symmetry-breaking signals. By virtue of their short-range nature and their capacity to activate both lineage-specifying and cell-polarizing intracellular signaling cascades, Wnts can polarize cells at their site of contact, orienting the axis of cell division while simultaneously programming daughter cells to adopt diverging fates in a spatially stereotyped way. By coupling cell fate to position, symmetry-breaking Wnt signals were pivotal in constructing the metazoan body by generating cellular diversity and spatial form.
Irreversible processes are the source of order: hence 'order out of chaos.' Processes associated with randomness (openness) lead to higher levels of organisation. Under certain conditions, entropy may thus become the progenitor of order. The authors propose a vast synthesis that embraces both reversible and irreversible time, and show how they relate to one another at both macroscopic and minute levels of examination.-A.Toffler
One of the central goals in biology is to understand how and how much of the phenotype of an organism is encoded in its genome. Although many genes that are crucial for organismal processes have been identified, much less is known about the genetic bases underlying quantitative phenotypic differences in natural populations. We discuss the fundamental gap between the large body of knowledge generated over the past decades by experimental genetics in the laboratory and what is needed to understand the genotypeto- phenotype problem on a broader scale. We argue that systems genetics, a combination of systems biology and the study of natural variation using quantitative genetics, will help to address this problem. We present major advances in these two mostly disconnected areas that have increased our understanding of the developmental processes of flowering time control and root growth. We conclude by illustrating and discussing the efforts that have been made toward systems genetics specifically in plants. Expected final online publication date for the Annual Review of Cell and Developmental Biology Volume 32 is October 06, 2016. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
Since its origin from inorganic matter, biological life undoubtedly has gained complexity. Evidence of this can be found in the lineage of the Viridiplantae or Chlorobionta (“green plants”), represented by the extant diversity of green algae and land plants. The land plants, together with the multicellular animals, arguably represent the two most complex groups of organisms on earth. For both groups, a correlation between the observable morphological complexity and the regulatory networks principally controlling it has been hypothesized. Both groups of organisms not only independently evolved multicellularity, but also underwent ancestral whole genome duplication events that presumably acted as evolutionary playgrounds for the expansion of regulatory and morphological complexity. Within animals, multicellularity evolved once and most genome duplications occurred hundreds of millions of years ago. However, an entirely different scenario unfolds among the Viridiplantae: multicellularity evolved several times independently within the green lineage, and genome duplication is the rule rather than the exception and continues to be utilized. The most successful flavor of green multicellularity evolved within the last common ancestor of extant land plants and their sister group, the charophyte algae. In this chapter, we will review common complexity concepts, introduce and compare means to quantify them, and discuss how the evolution of morphological complexity, as measured by gene regulatory complexity, distinctively affected terrestrial plants and the predominantly aquatic green, red and brown algae.
Hox gene clusters of jaw vertebrates display a tight genomic organization, which has no equivalent in any other bilateria genomes sequenced thus far. It was previously argued that such a topological consolidation toward a condensed, metagenic structure was due to the accumulation of long-range regulations flanking Hox loci, a phenomenon made possible by the successive genome duplications that occurred at the root of the vertebrate lineage, similar to gene neofunctionalization but applied to a coordinated multigenic system. Here, we propose that the emergence of such large vertebrate regulatory landscapes containing a range of global enhancers was greatly facilitated by the presence of topologically associating domains (TADs). These chromatin domains, mostly constitutive, may have been used as genomic niches where novel regulations could evolve due to both the preexistence of a structural backbone poised to integrate novel regulatory inputs, and a highly adaptive transcriptional readout. We propose a scenario for the coevolution of such TADs and the emergence of pleiotropy at ancestral vertebrate Hox loci.
Over the past 25 years, new techniques, new discoveries, and new ideas have profoundly impacted our understanding of deuterostome interrelationships and, ultimately, deuterostome evolution. During the late 1980s and early 1990s morphological cladistic analyses made predictions about both taxonomic history and homology, predictions that would be tested independent of the morphological characters themselves with the advent of molecular systematics, the rise of evolutionary developmental biology, and continued exploration of the fossil record. Thanks to these three areas of inquiry, we have gone from scenarios where animals like mobile enteropneust hemichordates and chordates were derived from sessile filter-feeding animals like modern lophophorates, echinoderms, and pterobranch hemichordates, to a new perspective where hemichordates are recognized as the nearest living relative of the echinoderms, and that vagile gill-bearing animals like Cambrian vetulicolians are seen—at least by some—as close to the deuterostome last common ancestor, with both sessility and filter-feeding convergent features of deuterostomes (e.g., echinoderm) and non-deuterostomes (e.g., lophophorates) alike. Although much of the backbone of the new deuterostome phylogeny is supported by multiple independent data sets, as are statements of homology of several different morphological characters, in particular the homology of gill slits across Deuterostomia, nonetheless, the next quarter century of study on this remarkable group of animals promises to be as equally illuminating and exciting as the past quarter century.
In the late 1980s, researchers began applying molecular sequencing tools to questions of deep animal phylogeny. These advances in sequencing were accompanied with improvements in computation and phylogenetic methods, and served to significantly reshape our understanding of metazoan evolution. Prior to this time, researchers asserted phylogenetic hypotheses based on their experience with taxa and to some degree, their authority. Molecular phylogenetic tools provided discrete methods and objective characters for reconstructing phylogeny. Nonetheless, major changes to widely accepted views, such as animal phylogeny, take time to be accepted. Development and acceptance of our current understanding of animal evolution occurred in three main phases: initial hypotheses based on 18S data, confirmation with additional molecular markers, and continued refinement with phylogenomics. With the advent of ideas such as Lophotrochozoa and Ecdysozoa, flaws in the traditional view became apparent. We now understand that complex morphological and embryological features (e.g., segmentation, coelom formation, development of body cavities) are much more evolutionarily plastic than previously recognized. Here, I explore how the transition from the traditional to the modern phylogenetic understanding of animal phylogeny occurred and examine some implications of this change in understanding. As the field moves forward, the utility of morphological and embryological characters for reconstruction of deep animal phylogeny should be discouraged. Instead, these characters should be interpreted in the light of independent phylogeny.
Hemocyte aggregation immediately following hemolymph withdrawal from the scallop Mizuhopecten yessoensis was studied using scanning electron microscopy, histological techniques, microphotography, and cytochalasin treatment. In the course of hemocyte aggregation that had started during hemolymph withdrawal, the originally loose flake-like aggregates became spherically shaped within 1-1.5 h. Aggregate contraction was inhibited by cytohalasin treatment. Hemocytes in the lower part of each aggregate were attached to the substrate, and after aggregate contraction, they spread over the surface, thus representing a print of the original shape of aggregate.