ON THE EVOLUTION OF DIFFERENTIATED MULTICELLULARITY

Most conspicuous organisms are multicellular and most multicellular organisms develop somatic cells to perform specific, nonreproductive tasks. The ubiquity of this division of labor suggests that it is highly advantageous. In this article I present a model to study the evolution of specialized cells. The model allows for unicellular and multicellular organisms that may contain somatic (terminally differentiated) cells. Cells contribute additively to a quantitative trait. The fitness of the organism depends on this quantitative trait (via a benefit function), the size of the organism, and the number of somatic cells. The model allows one to determine when somatic cells are advantageous and to calculate the optimum number (or fraction) of reproductive cells. I show that the fraction of reproductive cells is always surprisingly high. If somatic cells are very small, they can outnumber reproductive cells but their biomass is still less than the biomass of reproductive cells. I discuss the biology of primitive multicellular organisms with respect to the model predictions. I find a good agreement and outline how this work can be used to guide further quantitative studies of multicellularity.     

Competition between plasmid-bearing and plasmid-free organisms in a chemostat with nutrient recycling and an inhibitor

The asymptotic behavior of solutions of a model for competition between plasmid-bearing and plasmid-free organisms in the chemostat with two distributed delays and an external inhibitor is considered. The model presents a refinement of the one considered by Lu and Hadeler [Z. Lu, K.P. Hadeler, Model of plasmid-bearing plasmid-free competition in the chemostat with nutrient recycling and an inhibitor, Math. Biosci. 167 (2000) p. 177]. The delays model the fact that the nutrient is partially recycled after the death of the biomass by bacterial decomposition. Furthermore, it is assumed that there is inter-specific competition between the plasmid-bearing and plasmid-free organisms as well as intra-specific competition within each population. Conditions for boundedness of solutions and existence of non-negative equilibrium are given. Analysis of the extinction of the organisms, including plasmid-bearing and plasmid-free organisms, and the uniform persistence of the system are also carried out. By constructing appropriate Liapunov-like functionals, some sufficient conditions of global attractivity to the extinction equilibria are obtained and the combined effects of the delays and the inhibitor are studied.     

Spatial interactions within modular organisms: genetic heterogeneity and organism fitness

Modular organisms are composed of iterated units of construction that vary in their spatial arrangement. This variation is expected to affect the fitness of modular organisms due to interactions among neighboring modules and the potential for such organisms to be genetically heterogeneous. We devise a spatially explicit model to investigate how spatial interactions among neighboring modules affect organism fitness. We show that fitness is strongly dependent on the spatial arrangement of modules in both genetically homogeneous and heterogeneous organisms, and that the magnitude of the variation is dependent on the strength of interactions among modules. Organism fitness is more variable with interactions among modules that are symmetrical (each affects each other in the same directions) than with asymmetrical interactions (neighbors affect each other in different directions). We conclude by discussing potential extension of the present framework to a general dynamic model of spatially structured organism development.     

From disease to development to cell biology and back

Nowadays, the focus of developmental studies is shifting away from formal models of developmental pathways that are characterised by flow charts of controlling factors connected by arrows, to mechanistic models that explain developmental processes at the cellular level. Surprisingly, this shift towards a cellular view of developmental biology is occurring simultaneously across a range of model organisms. One consequence of taking such a cell biological view of development is that many model organisms are now becoming good models for studies of human disease and therapy.     

Idealization in evolutionary developmental investigation: a tension between phenotypic plasticity and normal stages

Idealization is a reasoning strategy that biologists use to describe, model and explain that purposefully departs from features known to be present in nature. Similar to other strategies of scientific reasoning, idealization combines distinctive strengths alongside of latent weaknesses. The study of ontogeny in model organisms is usually executed by establishing a set of normal stages for embryonic development, which enables researchers in different laboratory contexts to have standardized comparisons of experimental results. Normal stages are a form of idealization because they intentionally ignore known variation in development, including variation associated with phenotypic plasticity (e.g. via strict control of environmental variables). This is a tension between the phenomenon of plasticity and the practice of staging that has consequences for evolutionary developmental investigation because variation is conceptually removed as a part of rendering model organisms experimentally tractable. Two compensatory tactics for mitigating these consequences are discussed: employing a diversity of model organisms and adopting alternative periodizations.     

Genome‐enabled development of DNA markers for ecology,evolution and conservation

Molecular markers have become a fundamental piece of modern biology’s toolkit. In the last decade, new genomic resources from model organisms and advances in DNA sequencing technology have altered the way that these tools are developed, alleviating the marker limitation that researchers previously faced and opening new areas of research for studies of non‐model organisms. This availability of markers is directly responsible for advances in several areas of research, including fine‐scaled estimation of population structure and demography, the inference of species phylogenies, and the examination of detailed selective pressures in non‐model organisms. This review summarizes methods for the development of large numbers of DNA markers in non‐model organisms, the challenges encountered when utilizing different methods, and new research applications resulting from these advances.     

A rule-based approach to the modelling of bacterial ecosystems

This paper presents an approach to ecological/evolutionary modelling that is inspired by natural bacterial ecosystems and bacterial evolution. An individual-based artificial ecosystem model is proposed, which is designed to explore the evolvability of adaptive behavioural strategies in artificial bacteria represented by rule-based learning classifier systems. The proposed ecosystem model consists of a n-dimensional environmental grid, which can contain different types of artificial resources in arbitrary arrangements. The resources provide the energy that is necessary for the organisms to sustain life, and can trigger different types of behaviour in the organisms, such as movement towards nutrients and away from toxic substances, growth, and the controlled release of signalling resources. The balance between energy and material is modelled carefully to ensure that the ecosystem is dissipative. Those organisms that are able to efficiently exploit the available resources gradually accumulate enough energy to reproduce (by binary fission) and generate copies of themselves in the environment. Organisms are also able to produce their own resources, which can potentially be used as markers to send signals to other organisms (a behaviour known as quorum sensing). The complex relationships between stimuli and actions in the organisms are stochastically altered by means of mutations, thus enabling the organisms to adapt to their environment and maximise their lifespan and reproductive success. In this paper, the proposed bacterial ecosystem model is defined formally and its structure is discussed in detail. This is followed by results from simulation experiments that illustrate the model's operation and how it can be used in evolutionary modelling/computing scenarios.     

Darwinian selection leads to Gaia

The Gaia hypothesis, in its strongest form, states that the Earth's atmosphere, oceans, and biota form a tightly coupled system that maintains environmental conditions close to optimal for life. According to Gaia theory, optimal conditions are intrinsic, immutable properties of living organisms. It is assumed that the role of Darwinian selection is to favor organisms that act to stabilize environmental conditions at these optimal levels. In this paper, an alternative form of Gaia theory based on more traditional Darwinian principles is proposed. In the new approach, environmental regulation is a consequence of population dynamics, not Darwinian selection. The role of selection is to favor organisms that are best adapted to prevailing environmental conditions. However, the environment is not a static backdrop for evolution, but is heavily influenced by the presence of living organisms. The resulting co-evolving dynamical process eventually leads to the convergence of equilibrium and optimal conditions. A simple Daisyworld model is used to illustrate this convergence phenomenon. Sensitivity analysis of the Daisyworld model suggests that in stable ecosystems, the convergence of equilibrium and optimal conditions is inevitable, provided there are no externally driven shocks to the system. The end result may appear to be the product of a cooperative venture, but is in fact the outcome of Darwinian selection acting upon "selfish" organisms.     

The choice of model organisms in evo-devo

Study of the model organisms of developmental biology was crucial in establishing evo-devo as a new discipline. However, it has been claimed that this limited sample of organisms paints a biased picture of the role of development in evolution. Consequently, judicious choice of new model organisms is necessary to provide a more balanced picture. The challenge is to determine the best criteria for choosing new model organisms, given limited resources.     

Phylogenetic context and Basal metazoan model systems

In comparative studies using model organisms, extant taxa areoften referred to as basal. The term suggests that such taxaare descendants of lineages that diverged early in the historyof some larger taxon. By this usage, the basal metazoans comprisejust four phyla (Placozoa, Porifera, Cnidaria, and Ctenophora)and the large clade Bilateria. We advise against this practicebecause basal refers to a region at the base or root of a phylogenetictree. Thus, referring to an extant taxon or species as basal,or as more basal than another, can be misleading. While muchprogress has been made toward understanding some of the phylogeneticrelationships within these groups, the relationships among themare still largely not known with certainty. Thus, sound inferencesfrom comparative studies of model organisms demand continuedillumination of phylogeny. Hypotheses about the mechanisms underlyingmetazoan evolution can be drawn from the study of model organismsin Cnidaria, Ctenophora, Placozoa, and Porifera, but it is clearthat these model organisms are likely to be derived in manyrespects. Therefore, testing these hypotheses requires the studyof yet additional model organisms. The most effective testsare those that investigate model organisms with phylogeneticpositions among two sister groups comprising a larger cladeof interest.     

The Manna Effect: A Model of Phytoplankton Patchiness in a Regenerative System

A Monte Carlo model for the growth of phytoplankton in a regenerative system has been constructed. This model assumes that nutrients are regenerated randomly in time and space at the scale which is important to the individual organisms. Under such a regime, organisms originally arrayed in a random fashion assume a patchy distribution within fifteen or twenty divisions, with some species becoming nonrandom in their distribution within five divisions. Other factors, physical or biological, may also induce or enhance patchiness, but normal regenerative processes in a nutrient-limited system are sufficient in themselves to explain the phenomenon. Patchiness should be considered as the normal state for nonmotile organisms.     

Saccharomyces cerevisiae as a model organism: a comparative study

Background

Model organisms are used for research because they provide a framework on which to develop and optimize methods that facilitate and standardize analysis. Such organisms should be representative of the living beings for which they are to serve as proxy. However, in practice, a model organism is often selected ad hoc, and without considering its representativeness, because a systematic and rational method to include this consideration in the selection process is still lacking.

Methodology/Principal Findings

In this work we propose such a method and apply it in a pilot study of strengths and limitations of Saccharomyces cerevisiae as a model organism. The method relies on the functional classification of proteins into different biological pathways and processes and on full proteome comparisons between the putative model organism and other organisms for which we would like to extrapolate results. Here we compare S. cerevisiae to 704 other organisms from various phyla. For each organism, our results identify the pathways and processes for which S. cerevisiae is predicted to be a good model to extrapolate from. We find that animals in general and Homo sapiens in particular are some of the non-fungal organisms for which S. cerevisiae is likely to be a good model in which to study a significant fraction of common biological processes. We validate our approach by correctly predicting which organisms are phenotypically more distant from S. cerevisiae with respect to several different biological processes.

Conclusions/Significance

The method we propose could be used to choose appropriate substitute model organisms for the study of biological processes in other species that are harder to study. For example, one could identify appropriate models to study either pathologies in humans or specific biological processes in species with a long development time, such as plants.     

Microbes modeling ontogeny

Model organisms are central to contemporary biology and studies of embryogenesis in particular. Biologists utilize only a small number of species to experimentally elucidate the phenomena and mechanisms of development. Critics have questioned whether these experimental models are good representatives of their targets because of the inherent biases involved in their selection (e.g., rapid development and short generation time). A standard response is that the manipulative molecular techniques available for experimental analysis mitigate, if not counterbalance, this concern. But the most powerful investigative techniques and molecular methods are applicable to single-celled organisms (‘microbes’). Why not use unicellular rather than multicellular model organisms, which are the standard for developmental biology? To claim that microbes are not good representatives takes us back to the original criticism leveled against model organisms. Using empirical case studies of microbes modeling ontogeny, we break out of this circle of reasoning by showing: (a) that the criterion of representation is more complex than earlier discussions have emphasized; and, (b) that different aspects of manipulability are comparable in importance to representation when deciding if a model organism is a good model. These aspects of manipulability harbor the prospect of enhancing representation. The result is a better understanding of how developmental biologists conceptualize research using experimental models and suggestions for underappreciated avenues of inquiry using microbes. More generally, it demonstrates how the practical aspects of experimental biology must be scrutinized in order to understand the associated scientific reasoning.     

Reproductive aging: insights from model organisms

Aging was once thought to be the result of a general deterioration of tissues as opposed to their being under regulatory control. However, investigations in a number of model organisms have illustrated that aspects of aging are controlled by genetic mechanisms and are potentially manipulable, suggesting the possibility of treatment for age-related disorders. Reproductive decline is one aspect of aging. In model organisms and humans of both sexes, increasing age is associated with both a decline in the number of progeny and an increased incidence of defects. The cellular mechanisms of reproductive aging are not well understood, although a number of factors, both intrinsic and extrinsic to an organism's germline, may contribute to aging phenotypes. Recent work in a variety of organisms suggests that nuclear organization and nuclear envelope proteins may play a role in these processes.     

Monogonont rotifers as model systems for the study of micro-evolutionary adaptation and its eco-evolutionary implications

A better understanding of the ability of organisms to adapt to local selection conditions is essential for a better insight in their ecological dynamics. The study of micro-evolutionary adaptation and its eco-evolutionary consequences is challenging for many reasons and the choice of a suitable model organism is particularly important. In this paper, we explain why monogonont rotifers, through their unique combination of traits, are ideal study organisms for this purpose. With a literature review, we demonstrate the capacity of monogonont populations to adapt to a variety of selection conditions (e.g., salinity, food shortage, elemental limitation, and disturbance regimes) within very short-time frames and highlight some potential eco-evolutionary implications. Although monogononts are increasingly used in eco-evolution-oriented studies, their potential is still underappreciated compared to other model organisms. No doubt the high prevalence of cryptic species complexes and the lack of genomic tools form important obstacles that may discourage researchers to work with this group. Here, we argue that none of these difficulties should prevent monogonont rotifers from becoming commonly used model organisms in micro-evolutionary studies and make suggestions for future research.     

From asexual to eusocial reproduction by multilevel selection by density-dependent competitive interactions

A game theoretical model is developed to illustrate that multilevel selection by density-dependent competitive interactions in mobile organisms might have played a major role in the evolutionary transitions from asexual over sexual to eusocial reproduction. The model has four equilibria with selection occurring among interacting units of respectively one, two, three, and up to infinitely many individuals. The different equilibria are characterised by different levels of competitive interactions among interacting units, and these levels select for different levels of sexual and co-operative reproduction among the individuals of the units. The model predicts: (i) that low-energy organisms with negligible body masses have asexual reproduction; (ii) that high-energy organisms with non-negligible body masses in evolutionary equilibria have sexual reproduction between a female and a male; (iii) that high-energy organisms with non-negligible body masses that increase exponentially at an evolutionary steady state have co-operative reproduction between a sexual pair and a single sexually produced offspring; and (iv) that high-energy organisms with upward constrained body masses have eusocial reproduction between a sexual pair and up to an infinite number of sexually produced offspring workers.     

Yeast and filamentous fungi as model organisms in microbody research

Yeast and filamentous fungi are important model organisms in microbody research. The value of these organisms as models for higher eukaryotes is underscored by the observation that the principles of various aspects of microbody biology are strongly conserved from lower to higher eukaryotes. This has allowed to resolve various peroxisome-related functions, including peroxisome biogenesis disorders in man. This paper summarizes the major advances in microbody research using fungal systems and specifies specific properties and advantages/disadvantages of the major model organisms currently in use.     

Stages in the development of a model organism as a platform for mechanistic models in developmental biology: Zebrafish, 1970-2000

Model organisms became an indispensable part of experimental systems in molecular developmental and cell biology, constructed to investigate physiological and pathological processes. They are thought to play a crucial role for the elucidation of gene function, complementing the sequencing of the genomes of humans and other organisms. Accordingly, historians and philosophers paid considerable attention to various issues concerning this aspect of experimental biology. With respect to the representational features of model organisms, that is, their status as models, the main focus was on generalization of phenomena investigated in such experimental systems. Model organisms have been said to be models for other organisms or a higher taxon. This, however, presupposes a representation of the phenomenon in question. I will argue that prior to generalization, model organisms allow researchers to built generative material models of phenomena - structures, processes or the mechanisms that explain them - through their integration in experimental set-ups that carve out the phenomena from the whole organism and thus represent them. I will use the history of zebrafish biology to show how model organism systems, from around 1970 on, were developed to construct material models of molecular mechanisms explaining developmental or physiological processes.     

Conservation of a Pumilio-Nanos complex from<Emphasis Type="Italic"> Drosophila</Emphasis> germ plasm to human germ cells

Germ cells are the cells which ultimately give rise to mature sperm and eggs. In model organisms such as flies and worms, several genes that are required for formation and maintenance of germ cells have been identified and their interactions are rapidly being delineated. By contrast, little is known of the genes required for development of human germ cells and it is not clear whether findings from model organisms will translate into knowledge of human germ cell development, especially given observations that reproductive pathways may evolve more rapidly than somatic pathways. The Pumilio and Nanos genes have been especially well-characterized in model organisms and encode proteins that interact and are required for development of germ stem cells in one or both sexes. Here we report the first characterization of a mammalian Nanos homolog, human NANOS1 ( NOS1). We show that human NOS1 protein interacts with the human PUMILIO-2 (PUM2) protein via highly conserved domains to form a stable complex. We also show that in men, the NOS1 and PUM2 proteins are particularly abundant in germline stem cells. These observations mirror those in distant species and document for the first time a conserved protein-protein interaction in germ cells from flies to humans. These results suggest the possibility that the interaction of PUM2 and NOS1 may play a conserved role in germ cell development and maintenance in humans as in model organisms.