Evolutionary cell biology: two origins, one objective

Through a comparative approach, evolutionary cell biology makes use of genomics, bioinformatics, and cell biology of non-model eukaryotes to provide new avenues for understanding basic cellular processes. This approach has led to proposed mechanisms underpinning the evolution of eukaryotic cellular organization including endosymbiotic and autogenous processes and neutral and adaptive processes. Together these mechanisms have contributed to the genesis and complexity of organelles, molecular machines, and genome architecture. We review these mechanisms and suggest that a greater appreciation of the diversity in eukaryotic form has led to a more complete understanding of the evolutionary connections between organelles and the unexpected routes by which this diversity has been reached.

In this theory, cell di€erentiation is a two-step mechanism at each stage of development. In the ®rst step, gene expression is unstable. It occurs stochastically and produces di€erent cell types. In the second step gene expression is stabilized by means of cellular interactions. However, this stabilization cannot occur until the combination of cell phenotypes corresponding to the developmental stage is expressed. This selection mechanism prevents disorganizing consequences of stochasticity in gene expression and directs the embryo towards the adult stage. Instability and stochasticity in gene expression are caused by random displacement of regulators along DNA, whereas phosphorylation and/or dephos-phorylation of transcriptional regulators triggered by signal transduction between cells are responsible for the stabilization of stochastic gene expression. The origin of cellular di€erentiation is explained as an adaptation of cells to metabolic gradients created by substrate di€u-sion inside growing cell populations. This mechanism provides cells with complementary metabolism, increasing their ability to use food resources. Because the metabolic gradients are dependent on external substrate concentrations, cellular di€erentiation can also be viewed as an extension of natural selection inside organisms .

This article offers a novel, enlightened concept for determining the mechanism of evolution. It is based on homeostasis, which distinguishes life from nonlife and as such is the universal mechanism for the evolution of all living organisms. This view of evolution is logical, mechanistic, non-scalar, predictive, testable, and falsifiable, and it illuminates the epistemological relationships between physics and biology, ontogeny and phylogeny, development and aging, ultimate and proximate causation, health and disease. In addition to validating Haeckel's biogenetic law and Lamarckian epigenetics, reflecting the enabling value of the cellular approach, this perspective also expresses the evolutionary process at the cell-molecular level, since the mechanism of cell communication itself is universal in biology, in keeping with a Kuhnian paradigm shift. This approach may even elucidate the nature and evolution of consciousness as a manifestation of the cellular continuum from unicellular to multicellular life. We need such a functional genomic mechanism for the process of evolution if we are to make progress in biology and medicine. Like Copernican heliocentrism, a cellular approach to evolution may fundamentally change humankind's perceptions about our place in the universe.

2014

The problem of unicellular-multicellular transition is one of the main issues that is discussing in evolutionary biology. In [1] the fitness of a colony of cells is considered in terms of its two basic components, viability and fecundity. Intrinsic trade-off function of each cell defines a type of cell. We elaborate models providing in [1]. Assuming that all intrinsic trade-off functions are linear, we construct a model with different cell types and show that the differentiation of these types tends to full specialization. In addition, we attempt to consider the fact that environmental factors influence on the fitness of the colony. Thus, we introduce an energy restriction to the model and show that in optimum we get situations in which there exists a set of states, each of them allowing colony to achieve the same maximum level of fitness. In some states arbitrary chosen cell may be specialized, in some - unspecialized, but fecundity and viability of each cell belong to limited rang...

Cell Communication Insights, 2009

In the post-genomic era the complex problem of evolutionary biology can be tackled from the top-down, the bottom-up, or from the middle-out. Given the emergent and contingent nature of this process, we have chosen to take the latter approach, both as a mechanistic link to developmental biology and as a rational means of identifying signaling mechanisms based on their functional genomic significance. Using this approach, we have been able to configure a working model for lung evolution by reverse-engineering lung surfactant from the mammalian lung to the swim bladder of fish. Based on this archetypal cell-molecular model, we have reduced evolutionary biology to cell communication, starting with unicellular organisms communicating with the environment, followed by cell-cell communication to generate metazoa, culminating in the communication of genetic information between generations, i.e. reproduction. This model predicts the evolution of physiologic systems-including development, homeostasis, disease, regeneration/ repair, and aging-as a logical consequence of biology reducing entropy. This approach provides a novel and robust way of formulating refutable, testable hypotheses to determine the ultimate origins and first principles of physiology, providing candidate genes for phenotypes hypothesized to have mediated evolutionary changes in structure and/or function. Ultimately, it will form the basis for predictive medicine and molecular bioethics, rather than merely showing associations between genes and pathology, which is an unequivocal Just So Story. In this new age of genomics, our reach must exceed our grasp.

Proceedings of the National Academy of Sciences, 2012

Although observations from biochemistry and cell biology seemingly illustrate hundreds of examples of exquisite molecular adaptations, the fact that experimental manipulation can often result in improvements in cellular infrastructure raises the question as to what ultimately limits the level of molecular perfection achievable by natural selection. Here, it is argued that random genetic drift can impose a strong barrier to the advancement of molecular refinements by adaptive processes. Moreover, although substantial improvements in fitness may sometimes be accomplished via the emergence of novel cellular features that improve on previously established mechanisms, such advances are expected to often be transient, with overall fitness eventually returning to the level before incorporation of the genetic novelty. As a consequence of such changes, increased molecular/cellular complexity can arise by Darwinian processes, while yielding no long-term increase in adaptation and imposing increased energetic and mutational costs.

Cellular and Molecular Life Sciences, 2021

The extent to which normal (nonmalignant) cells of the body can evolve through mutation and selection during the lifetime of the organism has been a major unresolved issue in evolutionary and developmental studies. On the one hand, stable multicellular individuality seems to depend on genetic homogeneity and suppression of evolutionary conflicts at the cellular level. On the other hand, the example of clonal selection of lymphocytes indicates that certain forms of somatic mutation and selection are concordant with the organism-level fitness. Recent DNA sequencing and tissue physiology studies suggest that in addition to adaptive immune cells also neurons, epithelial cells, epidermal cells, hematopoietic stem cells and functional cells in solid bodily organs are subject to evolutionary forces during the lifetime of an organism. Here we refer to these recent studies and suggest that the expanding list of somatically evolving cells modifies idealized views of biological individuals as radically different from collectives.

Origins of Life and Evolution of Biospheres, 2007

Inventories of the gene content of the last common ancestor (LCA), i.e., the cenancestor, include sequences that may have undergone horizontal transfer events, as well as sequences that have originated in different pre-cenancestral epochs. However, the universal distribution of highly conserved genes involved in RNA metabolism provide insights into early stages of cell evolution during which RNA played a much more conspicuous biological role, and is consistent with the hypothesis that extant living systems were preceded by an RNA/protein world. Insights into the traits of primitive entities from which the LCA evolved may be derived from the analysis of paralogous gene families, including those formed by sequences that resulted from internal elongation events. Three major types of paralogous gene families can be recognized. The importance of this grouping for understanding the traits of early cells is discussed.

BioEssays

Understanding the evolutionary role of environmentally-induced phenotypic variation (i.e., environmental plasticity) is an important issue in developmental evolution. One of the major physiological responses to environmental changes is cellular stress, which is counteracted by a generic stress reaction that detoxifies the cell, refolds proteins, and repairs DNA damage. In this paper, we elaborate on a previous finding suggesting that the cell differentiation cascade of human decidual stromal cells, a cell type critical for embryo implantation and the maintenance of pregnancy, evolved from a cellular stress reaction. We hypothesize that the stress reaction in these cells was elicited ancestrally through the inflammation caused by embryo attachment and invasion. We describe a model, Stress-Induced Evolutionary Innovation (SIEI), whereby ancestral stress reactions and their corresponding pathways can be transformed into novel structural components of body plans, such as new cell types. After reviewing similarities and differences between SIEI and the "plasticity first hypothesis" (PFH) of evolution, we argue that SIEI is a distinct form of plasticity-based evolutionary change because it leads to the origin of novel structures rather than the adaptive transformation of a pre-existing character.

Artificial Life and Robotics, 1999

Evolution of ribonucleic acid (RNA) molecules in the test-tube provides a possibility to study evolutionary optimization and adaptation to the environment on time scales accessible to human observers. Diversity of genotypes, however, is prohibitive for a complete experimental recording of the process on the molecular level. The number of RNA sequences and structures is too large to be determined by means of currently available techniques. Computer simulation, in contrary, is able to handle large numbers of individual sequences and has no major problem with data retrieval. However, it can deal only with simpli ed relations between genotypes and phenotypes, being RNA sequences and structures, respectively. Based on a course-grained notion of structure, as represented by RNA secondary structures, for example, a comprehensive model of evolution has been developed that allows to follow optimization at full molecular resolution. This model describes the course of in vitro selection experiments and provides a straightforward explanation for the occurrence of steps observed in evolution. It initiated the development of new mathematical concepts which analyse evolution as a complex process viewed simultaneously in concentration space, sequence space and shape space.

Integrative and Comparative Biology, 1990

SYNOPSIS. Biologists are integrating studies of morphology, development, physiology, and other disciplines in order to understand how species and lineages diversify and cope with their environments. An evolutionary perspective in such studies, including those of cells, tissues, and organs, is potentially useful for the structure and analysis of such problems. Evolutionary biology is the study of the history of evolution and the elucidation of its mechanisms. Comparative biology is the comparison of a trait or traits in selected taxa, and may be, but need not be, evolutionary in approach. A phylogenetic hypothesis is necessary for reconstruction of pattern in morphology, ecology, behavior, and other areas. Acquaintance with evolutionary and phylogenetic perspectives can guide selection of taxa for study and open new approaches to analysis of data. Such an approach is not always appropriate to problems in biology, but it could be utilized beneficially more frequently than is currently practiced. Studies of cells, tissues, and organs may contribute to the construction of new phylogenetic hypotheses and to analysis of patterns and mechanisms of change when pursued from an evolutionary perspective.

Toward a theory of development, 2014

postulated the existence of a highly organized microscopic material structure in the germinal cells that he called 'germinative plasma'. This structure, which foreshadowed DNA, was thought to control development in a very precise way, with each of its parts determining a part of the adult organism (Weismann, 1891).

BioEssays

Origins and Evolution of Life

Biological cells present a paradox, in that they show simultaneous stability and flexibility, allowing them to adapt to new environments and to evolve over time. The emergence of stable cell states depends on genotype-to-phenotype associations, which essentially reflect the organization of gene regulatory modes. The view taken here is that cell-state organization is a dynamical process in which the molecular disorder manifests itself in a macroscopic order. The genome does not determine the ordered cell state; rather, it participates in this process by providing a set of constraints on the spectrum of regulatory modes, analogous to boundary conditions in physical dynamical systems. We have developed an experimental framework, in which cell populations are exposed to unforeseen challenges; novel perturbations they had not encountered before along their evolutionary history. This approach allows an unbiased view of cell dynamics, uncovering the potential of cells to evolve and develop adapted stable states. In the last decade, our experiments have revealed a coherent set of observations within this framework, painting a picture of the living cell that in many ways is not aligned with the conventional one. Of particular importance here, is our finding that adaptation of cell-state organization is essentially an efficient exploratory dynamical process rather than one founded on random mutations. Based on our framework, a set of concepts underlying cell-state organization—exploration evolving by global, non-specific, dynamics of gene activity—is presented here. These concepts have significant consequences for our understanding of the emergence and stabilization of a cell phenotype in diverse biological contexts. Their implications are discussed for three major areas of biological inquiry: evolution, cell differentiation and cancer. There is currently no unified theoretical framework encompassing the emergence of order, a stable state, in the living cell. Hopefully, the integrated picture described here will provide a modest contribution towards a physics theory of the cell.