Does resource availability help determine the evolutionary route to multicellularity?

Genetic heterogeneity and homogeneity are associated with distinct sets of adaptive advantages and bottlenecks, both in developmental biology and population genetics. Whereas populations of individuals are usually genetically heterogeneous, most multicellular metazoans are genetically homogeneous. Observing that resource scarcity fuels genetic heterogeneity in populations, we propose that monoclonal development is compatible with the resource-rich and stable internal environments that complex multicellular bodies offer. In turn, polyclonal development persists in tumors and in certain metazoans, both exhibiting a closer dependence on external resources. This eco-evo-devo approach also suggests that multicellularity may originally have emerged through polyclonal development in early metazoans, because of their reduced shielding from environmental fluctuations.

Many roads lead to Rome: Neutral phenotypes in microorganisms.

John Bonner pointed out that microorganisms differ in several ways, some of which may reflect neutral phenotypic evolution. For making his case, Bonner referred to interspecies differences and morphological traits. Here we consider intraspecies differences and physiological traits. As a case-study, we examine the production of an extracellular cyclic 3 ' ,5 ' monophosphate phosphodiesterase in the cellular slime mold Dictyostelium discoideum. Temporal profiles of phosphodiesterase activity differ significantly between wild-type strains. From that we argue that the inference drawn initially from studies on a single wild-type, namely that the profile displayed by it pointed to an adaptive role, was mistaken. We generalize the conclusion to suggest that physiological differences exhibited by microorganisms of the same species may, but need not, reflect adaptations to different environments. Rather, the differences could be related to the fact that microorganisms live in groups whose composition can vary between homogeneous (clonal) and heterogeneous (polyclonal). More than one physiological profile is consistent with the normal development of the group in a given environment; the alternatives are neutral. When studying microbial physiology and behavior, it is expected that the observations are made on a clonal population; genetic (and so phenotypic) heterogeneity is carefully guarded against. As the example from D. discoideum shows, an unintended consequence of overlooking phenotypic heterogeneity is that one can fall into the trap of accepting a seemingly plausible, but possibly erroneous, adaptive explanation for a "normal" wild-type phenotype.

John Tyler Bonner: Remembering a scientific pioneer.

Throughout his life, John Tyler Bonner contributed to major transformations in the fields of developmental and evolutionary biology. He pondered the evolution of complexity and the significance of randomness in evolution, and was instrumental in the formation of evolutionary developmental biology. His contributions were vast, ranging from highly technical scientific articles to numerous books written for a broad audience. This historical vignette gathers reflections by several prominent researchers on the greatness of John Bonner and the implications of his work.

Phenotypic variability in unicellular organisms: from calcium signalling to social behaviour.

Historically, research has focused on the mean and often neglected the variance. However, variability in nature is observable at all scales: among cells within an individual, among individuals within a population and among populations within a species. A fundamental quest in biology now is to find the mechanisms that underlie variability. Here, we investigated behavioural variability in a unique unicellular organism, Physarum polycephalum. We combined experiments and models to show that variability in cell signalling contributes to major differences in behaviour underpinning some aspects of social interactions. First, following thousands of cells under various contexts, we identified distinct behavioural phenotypes: 'slow-regular-social', 'fast-regular-social' and 'fast-irregular-asocial'. Second, coupling chemical analysis and behavioural assays we found that calcium signalling is responsible for these behavioural phenotypes. Finally, we show that differences in signalling and behaviour led to alternative social strategies. Our results have considerable implications for our understanding of the emergence of variability in living organisms.

How many initiator tRNA genes does Escherichia coli need?

Multiple copies of a gene require enhanced investment on the part of the cell and, as such, call for an explanation. The observation that Escherichia coli has four copies of initiator tRNA (tRNAi) genes, encoding a special tRNA (tRNA(fMet)) required to start protein synthesis, is puzzling particularly because the cell appears to be unaffected by the removal of one copy. However, the fitness of an organism has both absolute and relative connotations. Thus, we carried out growth competition experiments between E. coli strains that differ in the number of tRNAi genes they contain. This has enabled us to uncover an unexpected link between the number of tRNAi genes and protein synthesis, nutritional status, and fitness. Wild-type strains with the canonical four tRNAi genes are favored in nutrient-rich environments, and those carrying fewer are favored in nutrient-poor environments. Auxotrophs behave as if they have a nutritionally poor internal environment. A heuristic model that links tRNAi gene copy number, genetic stress, and growth rate accounts for the findings. Our observations provide strong evidence that natural selection can work through seemingly minor quantitative variations in gene copy number and thereby impact organismal fitness.

Reflections on assortative mating, social stratification, and genetics.

A recent report by G. Clark points to a sustained persistence of social status in England that extends vertically across several generations and horizontally across many levels of kinship. We seek to put his findings in historical perspective. We do so by relating them to two lines of thinking related to biological inheritance. One predated the rediscovery of Mendel's work and led to the field of quantitative genetics, which dealt on the whole with quasi-continuously varying traits. The other is based on the rediscovery itself and led to a reconciliation between quantitative genetics and discrete Mendelian elements of heredity. Both were enmeshed with the supposed need for, and societal consequences of, eugenics and assortative mating. Also on both issues, the significant ideas can be traced to R. A. Fisher, inspired in one case by F. Galton and in the other by J. A. Cobb, with strong support for Galton and Cobb coming from Karl Pearson. Clark's findings point to societal stratification, and assortative mating for wealth is a straightforward hypothesis to account for it. However, it should be noted that the findings support, but do not prove, the hypothesis.

Hydrolysis of aromatic ß-glucosides by non-pathogenic bacteria confers a chemical weapon against predators.

Bacteria present in natural environments such as soil have evolved multiple strategies to escape predation. We report that natural isolates of Enterobacteriaceae that actively hydrolyze plant-derived aromatic ß-glucosides such as salicin, arbutin and esculin, are able to avoid predation by the bacteriovorous amoeba Dictyostelium discoideum and nematodes of multiple genera belonging to the family Rhabditidae. This advantage can be observed under laboratory culture conditions as well as in the soil environment. The aglycone moiety released by the hydrolysis of ß-glucosides is toxic to predators and acts via the dopaminergic receptor Dop-1 in the case of Caenorhabditis elegans. While soil isolates of nematodes belonging to the family Rhabditidae are repelled by the aglycone, laboratory strains and natural isolates of Caenorhabditis sp. are attracted to the compound, mediated by receptors that are independent of Dop-1, leading to their death. The ß-glucosides-positive (Bgl(+)) bacteria that are otherwise non-pathogenic can obtain additional nutrients from the dead predators, thereby switching their role from prey to predator. This study also offers an evolutionary explanation for the retention by bacteria of 'cryptic' or 'silent' genetic systems such as the bgl operon.

Ultradian rhythms: Life's dance to the music of time.

A recent and updated translation of a book, earlier published in Russian in 2021, contains a fascinating account of the development of a central theme in our understanding of the kinetics of cellular growth and development (Brodsky 2022). The book deals with the twin concepts of ultradian (i.e. about one hour period) signals and cellto-cell communication. The author, Vsevolod Ya. Brodsky, has performed a major service by discussing in a comprehensive manner studies on high-frequency oscillations in intercellular communication. The book will be especially valuable to readers who are not familiar with the extensive Russian literature on the subject, much of which has been ignored elsewhere. The present Commentary uses it as a take-off point in order to highlight issues that are common to the area of biological rhythms generally and ultradian oscillations in particular. In view of the importance of the book, we critique it towards the latter part of the Commentary in the style of a book review.

Genetic heterogeneity in wild isolates of cellular slime mold social groups.

This study addresses the issues of spatial distribution, dispersal, and genetic heterogeneity in social groups of the cellular slime molds (CSMs). The CSMs are soil amoebae with an unusual life cycle that consists of alternating solitary and social phases. Because the social phase involves division of labor with what appears to be an extreme form of "altruism", the CSMs raise interesting evolutionary questions regarding the origin and maintenance of sociality. Knowledge of the genetic structure of social groups in the wild is necessary for answering these questions. We confirm that CSMs are widespread in undisturbed forest soil from South India. They are dispersed over long distances via the dung of a variety of large mammals. Consistent with this mode of dispersal, most social groups in the two species examined for detailed study, Dictyostelium giganteum and Dictyostelium purpureum, are multi-clonal.

The past and present of developmental biology in India.

This issue of The International Journal of Developmental Biology (Int. J. Dev. Biol.) is devoted to contributions to developmental biology from India. The articles have been organized thematically, beginning with historical accounts and personal reminiscences, followed by surveys of areas to which the authors' own contributions have been substantial, and ending with reports of original research. The articles selected for the 'history' section are by those who have witnessed events from close quarters, and in most cases have contributed to the work in question. The range of articles is vast but cannot claim to be comprehensive. Some areas may have been left out inadvertently, either because we were unable to find anyone to cover them, or maybe in part because of not looking in the right place. Other areas are missed out because, much to our regret, authors did not deliver promised manuscripts on time. In short, the Special Issue is indicative of what went on and is going on in the field of developmental biology in India, but it does have gaps.

One of the most significant discoveries in Developmental Biology from an Indian laboratory - Iqbal A. Niazi and the role of retinoids in limb regeneration.

In this short commentary, we reflect upon the fascinating paper by I.A. Niazi entitled "Background to work on retinoids and amphibian limb regeneration: Studies on anuran tadpoles - a retrospect." originally published in J. Biosciences (1996), and herein reproduced with the kind permission of the author and the Journal of Biosciences. It is fitting that this landmark publication is included in this India-related Special Issue of the Int. J. Dev. Biol., because it sketches the background to what is arguably one of the two most significant discoveries in Developmental Biology to come from an Indian laboratory. Besides being of intrinsic interest, it spawned an entire area of research, one that deals with the role of retinoids in morphogenesis and development generally.

Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity.

Myxobacteria and dictyostelids are prokaryotic and eukaryotic multicellular lineages, respectively, that after nutrient depletion aggregate and develop into structures called fruiting bodies. The developmental processes and resulting morphological outcomes resemble one another to a remarkable extent despite their independent origins, the evolutionary distance between them and the lack of traceable homology in molecular mechanisms. We hypothesize that the morphological parallelism between the two lineages arises as the consequence of the interplay within multicellular aggregates between generic processes, physical and physicochemical processes operating similarly in living and non-living matter at the mesoscale (~10-3-10-1 m) and agent-like behaviors, unique to living systems and characteristic of the constituent cells, considered as autonomous entities acting according to internal rules in a shared environment. Here, we analyze the contributions of generic and agent-like determinants in myxobacteria and dictyostelid development and their roles in the generation of their common traits. Consequent to aggregation, collective cell-cell contacts mediate the emergence of liquid-like properties, making nascent multicellular masses subject to novel patterning and morphogenetic processes. In both lineages, this leads to behaviors such as streaming, rippling, and rounding-up, as seen in non-living fluids. Later the aggregates solidify, leading them to exhibit additional generic properties and motifs. Computational models suggest that the morphological phenotypes of the multicellular masses deviate from the predictions of generic physics due to the contribution of agent-like behaviors of cells such as directed migration, quiescence, and oscillatory signal transduction mediated by responses to external cues. These employ signaling mechanisms that reflect the evolutionary histories of the respective organisms. We propose that the similar developmental trajectories of myxobacteria and dictyostelids are more due to shared generic physical processes in coordination with analogous agent-type behaviors than to convergent evolution under parallel selection regimes. Insights from the biology of these aggregative forms may enable a unified understanding of developmental evolution, including that of animals and plants.

The trishanku gene and terminal morphogenesis in Dictyostelium discoideum.

Multicellular development in the social amoeba Dictyostelium discoideum is triggered by starvation. It involves a series of morphogenetic movements, among them being the rising of the spore mass to the tip of the stalk. The process requires precise coordination between two distinct cell types-presumptive (pre-) spore cells and presumptive (pre-) stalk cells. Trishanku (triA) is a gene expressed in prespore cells that is required for normal morphogenesis. The triA(-) mutant shows pleiotropic effects that include an inability of the spore mass to go all the way to the top. We have examined the cellular behavior required for the normal ascent of the spore mass. Grafting and mixing experiments carried out with tissue fragments and cells show that the upper cup, a tissue that derives from prestalk cells and anterior-like cells (ALCs), does not develop properly in a triA(-) background. A mutant upper cup is unable to lift the spore mass to the top of the fruiting body, likely due to defective intercellular adhesion. If wild-type upper cup function is provided by prestalk and ALCs, trishanku spores ascend all the way. Conversely, Ax2 spores fail to do so in chimeras in which the upper cup is largely made up of mutant cells. Besides proving that under these conditions the wild-type phenotype of the upper cup is necessary and sufficient for terminal morphogenesis in D. discoideum, this study provides novel insights into developmental and evolutionary aspects of morphogenesis in general. Genes that are active exclusively in one cell type can elicit behavior in a second cell type that enhances the reproductive fitness of the first cell type, thereby showing that morphogenesis is a cooperative process.

Individual and collective behaviour in cellular slime mould development: contributions of John Bonner (1920-2019).

John Bonner used the cellular slime moulds to address issues that lie at the heart of evolutionary and developmental biology. He did so mostly by combining acute observation and a knack for asking the right questions with the methods of classical embryology. The present paper focusses on his contributions to understanding two phenomena that are characteristic of development in general: chemotaxis of single cells to an external attractant, and spatial patterning and proportioning of cell types in the multicellular aggregate. Brief mention is also made of other areas of slime mould biology where he made significant inputs. He saw cellular slime moulds as exemplars of development and worthy of study in their own right. His ideas continue to inspire researchers.

An individual-level selection model for the apparent altruism exhibited by cellular slime moulds.

In Dictyostelium discoideum, cells that become part of the stalk or basal disc display behaviour that can be interpreted as altruistic. Atzmony et al. (Curr Sci 72:142-145, 1997) had hypothesised that this behaviour could be the outcome of an adaptive strategy based on differing intrinsic quality as reflected by phenotypes that indicate differences in potential for survival and reproduction, followed by intercellular competition among amoebae of differing qualities. Low-quality amoebae would have a poor chance of succeeding in the competition to form spores; they could enhance their chances of survival by adopting a presumptive stalk strategy. Here we extend the hypothesis by making use of recent findings. Our approach is based on the view that an evolutionary explanation for the apparent altruism of stalk cells in D. discoideum must apply broadly to other cellular slime moulds (CSMs) that exhibit stalk cell death. Further, it must be capable of being modified to cover social behaviour in CSMs with an extracellular stalk, as well as in sorocarpic amoebae whose stalk cells are viable. With regard to D. discoideum, we suggest that (a) differentiation-inducing factor, thought of as a signal that inhibits amoebae from forming spores and induces them to differentiate into basal disc cells, is better viewed as a mediator of competition among post-aggregation amoebae and (b) the products of the 'recognition genes', tgrB and tgrC, allow an amoeba to assess its quality relative to that of its neighbours and move to a position within the aggregate that optimises its reproductive fitness. From this perspective, all cells behave in a manner that is 'selfish' rather than 'altruistic', albeit with different expectations of success.

A New Classification of the Dictyostelids.

Traditional morphology-based taxonomy of dictyostelids is rejected by molecular phylogeny. A new classification is presented based on monophyletic entities with consistent and strong molecular phylogenetic support and that are, as far as possible, morphologically recognizable. All newly named clades are diagnosed with small subunit ribosomal RNA (18S rRNA) sequence signatures plus morphological synapomorphies where possible. The two major molecular clades are given the rank of order, as Acytosteliales ord. nov. and Dictyosteliales. The two major clades within each of these orders are recognized and given the rank of family as, respectively, Acytosteliaceae and Cavenderiaceae fam. nov. in Acytosteliales, and Dictyosteliaceae and Raperosteliaceae fam. nov. in Dictyosteliales. Twelve genera are recognized: Cavenderia gen. nov. in Cavenderiaceae, Acytostelium, Rostrostelium gen. nov. and Heterostelium gen. nov. in Acytosteliaceae, Tieghemostelium gen. nov., Hagiwaraea gen. nov., Raperostelium gen. nov. and Speleostelium gen. nov. in Raperosteliaceae, and Dictyostelium and Polysphondylium in Dictyosteliaceae. The "polycephalum" complex is treated as Coremiostelium gen. nov. (not assigned to family) and the "polycarpum" complex as Synstelium gen. nov. (not assigned to order and family). Coenonia, which may not be a dictyostelid, is treated as a genus incertae sedis. Eighty-eight new combinations are made at species and variety level, and Dictyostelium ammophilum is validated.

Ernst Mayr's interactions with J. B. S. Haldane.

Ernst Mayr and J. B. S. Haldane, major contributors to the 'modern synthesis' in evolutionary theory, set an example of how scientific disagreements need not come in the way of friendship. After getting acquainted, they kept discussing issues related to evolution until just before Haldane's death in 1964. Their dissimilar backgrounds meant that they adopted different approaches. A major disagreement emerged regarding the right way to look at the role of genes in evolution. Mayr felt that the elementary models of population genetics were oversimplifications and therefore inadequate for representing evolutionary processes, though he was not consistent in his attitude. Haldane, on the other hand, maintained that the mathematical treatment of simple models had an important role to play. The Mayr-Haldane interactions illustrate divergent viewpoints concerning the utility of mathematics in biology.

Calcium regulates the expression of a Dictyostelium discoideum asparaginyl tRNA synthetase gene.

In a screen for calcium-regulated gene expression during growth and development of Dictyostelium discoideum we have identified an asparaginyl tRNA synthetase (ddAsnRS) gene, the second tRNA synthetase gene identified in this organism. The ddAsnRS gene shows many unique features. One, it is repressed by lowering cellular calcium, making it the first known calcium-regulated tRNA synthetase. Two, despite the calcium-dependence, its expression is unaltered during the cell cycle, making this the first D. discoideum gene to show a calcium-dependent but cell cycle phase-independent expression. Finally, the N-terminal domain of the predicted ddAsnRS protein shows higher sequence similarity to Glutaminyl tRNA synthetases than to other Asn tRNA synthetases. These unique features of the AsnRS from this primitive eukaryote not only point to a novel mechanism regulating the components of translation machinery and gene expression by calcium, but also hint at a link between the evolution of GlnRS and AsnRS in eukaryotes.

Group behaviour in physical, chemical and biological systems.

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