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Deterministic actin waves as generators of cell polarization cues
Laboratoire Biologie cellulaire systémique de la polarité et de la division - Luiza Stankevicins, Nicolas Ecker, Emmanuel Terriac, Paolo Maiuri, Rouven Schoppmeyer, Pablo Vargas, Ana-Maria Lennon-Duménil, Matthieu Piel, Bin Qu, Markus Hoth, Karsten Kruse, and Franziska Lautenschläger
PNAS - 117 (2) 826-835 - doi.org/10.1073/pnas.1907845117 - 2020
Migration of cells can be characterized by two prototypical types of motion: individual and collective migration. We propose a statistical inference approach designed to detect the presence of cell-cell interactions that give rise to collective behaviors in cell motility experiments. This inference method has been first successfully tested on synthetic motional data and then applied to two experiments. In the first experiment, cells migrate in a wound-healing model: When applied to this experiment, the inference method predicts the existence of cell-cell interactions, correctly mirroring the strong intercellular contacts that are present in the experiment. In the second experiment, dendritic cells migrate in a chemokine gradient. Our inference analysis does not provide evidence for interactions, indicating that cells migrate by sensing independently the chemokine source. According to this prediction, we speculate that mature dendritic cells disregard intercellular signals that could otherwise delay their arrival to lymph vessels.
Pressure sensing through Piezo channels controls whether cells migrate with blebs or pseudopods
Laboratoire Biologie cellulaire systémique de la polarité et de la division - Nishit Srivastava, David Traynor, Matthieu Piel, Alexandre J. Kabla, and Robert R. Kay
PNAS - 117 (5) 2506-2512 - doi.org/10.1073/pnas.1905730117 - 2020
Cells migrating within the body perform vital functions in development and for defense and repair of tissues. In this dense environment, cells encounter mechanical forces and constraints not experienced when moving under buffer, and, accordingly, many change how they move. We find that gentle squashing, which mimics mechanical resistance, causes cells to move using blebs—a form of projection driven by fluid pressure—rather than pseudopods. This behavior depends on the Piezo stretch-operated ion channel in the cell membrane and calcium fluxes into the cell. Piezo is highly conserved and is required for light touch sensation; this work extends its functions into migrating cells.
Predicting Confined 1D Cell Migration from Parameters Calibrated to a 2D Motor-Clutch Model
Laboratoire Biologie cellulaire systémique de la polarité et de la division - Prahl LS, Stanslaski MR, Vargas P, Piel M, Odde DJ
Biophys. J. - 118(7) 1709-1720 - DOI: 10.1016/j.bpj.2020.01.048 - 2020
Biological tissues contain micrometer-scale gaps and pores, including those found within extracellular matrix fiber networks, between tightly packed cells, and between blood vessels or nerve bundles and their associated basement membranes. These spaces restrict cell motion to a single-spatial dimension (1D), a feature that is not captured in traditional in vitro cell migration assays performed on flat, unconfined two-dimensional (2D) substrates. Mechanical confinement can variably influence cell migration behaviors, and it is presently unclear whether the mechanisms used for migration in 2D unconfined environments are relevant in 1D confined environments. Here, we assessed whether a cell migration simulator and associated parameters previously measured for cells on 2D unconfined compliant hydrogels could predict 1D confined cell migration in microfluidic channels. We manufactured microfluidic devices with narrow channels (60-μm2 rectangular cross-sectional area) and tracked human glioma cells that spontaneously migrated within channels. Cell velocities (vexp = 0.51 ± 0.02 μm min-1) were comparable to brain tumor expansion rates measured in the clinic. Using motor-clutch model parameters estimated from cells on unconfined 2D planar hydrogel substrates, simulations predicted similar migration velocities (vsim = 0.37 ± 0.04 μm min-1) and also predicted the effects of drugs targeting the motor-clutch system or cytoskeletal assembly. These results are consistent with glioma cells utilizing a motor-clutch system to migrate in confined environments.
Centrosome–nuclear axis repositioning drives the assembly of a bipolar spindle scaffold to ensure mitotic fidelity
Laboratoire Biologie cellulaire systémique de la polarité et de la division - Vanessa Nunes, Margarida Dantas, Domingos Castro, Elisa Vitiello,e Irène Wang,e Nicolas Carpi, Martial Balland, Matthieu Piel, Paulo Aguiar, Helder Maiato, and Jorge G. Ferreira
Mol Biol Cell - 31(16) 1675–1690 - doi: 10.1091/mbc.E20-01-0047 - 2020
During the initial stages of cell division, the cytoskeleton is extensively reorganized so that a bipolar mitotic spindle can be correctly assembled. This process occurs through the action of molecular motors, cytoskeletal networks, and the nucleus. How the combined activity of these different components is spatiotemporally regulated to ensure efficient spindle assembly remains unclear. To investigate how cell shape, cytoskeletal organization, and molecular motors cross-talk to regulate initial spindle assembly, we use a combination of micropatterning with high-resolution imaging and 3D cellular reconstruction. We show that during prophase, centrosomes and nucleus reorient so that centrosomes are positioned on the shortest nuclear axis at nuclear envelope (NE) breakdown. We also find that this orientation depends on a combination of centrosome movement controlled by Arp2/3-mediated regulation of microtubule dynamics and Dynein-generated forces on the NE that regulate nuclear reorientation. Finally, we observe this centrosome configuration favors the establishment of an initial bipolar spindle scaffold, facilitating chromosome capture and accurate segregation, without compromising division plane orientation.
Cellular locomotion using environmental topography
Laboratoire Biologie cellulaire systémique de la polarité et de la division - Anne Reversat, Florian Gaertner, Jack Merrin, Julian Stopp, Saren Tasciyan, Juan Aguilera, Ingrid de Vries, Robert Hauschild, Miroslav Hons, Matthieu Piel, Andrew Callan-Jones, Raphael Voituriez, Michael Sixt
Nature - 582(7813) 582-585 - doi: 10.1038/s41586-020-2283-z. - 2020
Eukaryotic cells migrate by coupling the intracellular force of the actin cytoskeleton to the environment. While force coupling is usually mediated by transmembrane adhesion receptors, especially those of the integrin family, amoeboid cells such as leukocytes can migrate extremely fast despite very low adhesive forces1. Here we show that leukocytes cannot only migrate under low adhesion but can also transmit forces in the complete absence of transmembrane force coupling. When confined within three-dimensional environments, they use the topographical features of the substrate to propel themselves. Here the retrograde flow of the actin cytoskeleton follows the texture of the substrate, creating retrograde shear forces that are sufficient to drive the cell body forwards. Notably, adhesion-dependent and adhesion-independent migration are not mutually exclusive, but rather are variants of the same principle of coupling retrograde actin flow to the environment and thus can potentially operate interchangeably and simultaneously. As adhesion-free migration is independent of the chemical composition of the environment, it renders cells completely autonomous in their locomotive behaviour.
The impact of frost-damage on the quality and quantity of the secreted antigen-specific IgG repertoire
Laboratoire Colloïdes et Matériaux Divisés - Magda Rybczynska, Jean Baudrya, Eyer Klaus
ELSEVIER - 38(33) 5337-5342 - doi.org/10.1016/j.vaccine.2020.05.066 - 2020
Freezing of alum-based vaccines drastically alters their colloidal composition and leads to irreversible cluster formation. The loss of stability is well described, but the impact of frost damage on the functionality of the induced and secreted antibody repertoire has not been studied in detail. We therefore applied our single-cell measurement platform to extract the frequencies of Immunoglobulin G-secreting cells in combination with individual secretion rates and affinities. We showed that, frost-damaged or not, the tested vaccine was able to generate similar frequencies of total and antigen-affine IgG-secreting cells. Additionally, the frost-damaged vaccine stimulated a similar T-cell cytokine secretion pattern when compared to the regularly stored vaccine. However, frost-damaged vaccines induced no efficient affinity maturation and a complete collapse of the affinity distribution was observed. This study unveiled the impact of frost-damage to alum-based vaccines on the induced secreted antibody repertoire, and illustrated the power of functional single-antibody analysis.

Dynamic single-cell phenotyping of immune cells using the microfluidic platform DropMap
Laboratoire Colloïdes et Matériaux Divisés - Yacine Bounab, Klaus Eyer, Sophie Dixneuf, Magda Rybczynska, Cécile Chauvel, Maxime Mistretta, Trang Tran, Nathan Aymerich, Guilhem Chenon, Jean-François Llitjos, Fabienne Venet, Guillaume Monneret, Iain A. Gillespie, Pierre Cortez, Virginie Moucadel, Al
Nature Protocols - 15 2920–2955 - https://www.nature.com/articles/s41596-020-0354-0 - 2020
Characterization of immune responses is currently hampered by the lack of systems enabling quantitative and dynamic phenotypic characterization of individual cells and, in particular, analysis of secreted proteins such as cytokines and antibodies. We recently developed a simple and robust microfluidic platform, DropMap, to measure simultaneously the kinetics of secretion and other cellular characteristics, including endocytosis activity, viability and expression of cell-surface markers, from tens of thousands of single immune cells. Single cells are compartmentalized in 50-pL droplets and analyzed using fluorescence microscopy combined with an immunoassay based on fluorescence relocation to paramagnetic nanoparticles aligned to form beadlines in a magnetic field. The protocol typically takes 8–10 h after preparation of microfluidic chips and chambers, which can be done in advance. By contrast, enzyme-linked immunospot (ELISPOT), flow cytometry, time-of-flight mass cytometry (CyTOF), and single-cell sequencing enable only end-point measurements and do not enable direct, quantitative measurement of secreted proteins. We illustrate how this system can be used to profile downregulation of tumor necrosis factor-α (TNF-α) secretion by single monocytes in septic shock patients, to study immune responses by measuring rates of cytokine secretion from single T cells, and to measure affinity of antibodies secreted by single B cells.
The Quantitative Assessment of the Secreted IgG Repertoire after Recall to Evaluate the Quality of Immunizations
Laboratoire Colloïdes et Matériaux Divisés - Klaus Eyer, Carlos Castrillon, Guilhem Chenon, Jérôme Bibette, Pierre Bruhns, Andrew D. Griffiths and Jean Baudry
The Journal of Immunology - 205 8 - DOI: https://doi.org/10.4049/jimmunol.2000112 - 2020
One of the major goals of vaccination is to prepare the body to rapidly secrete specific Abs during an infection. Assessment of the vaccine quality is often difficult to perform, as simple measurements like Ab titer only partly correlate with protection. Similarly, these simple measurements are not always sensitive to changes in the preceding immunization scheme. Therefore, we introduce in this paper a new, to our knowledge, method to assay the quality of immunization schemes for mice: shortly after a recall with pure Ag, we analyze the frequencies of IgG-secreting cells (IgG-SCs) in the spleen, as well as for each cells, the Ag affinity of the secreted Abs. We observed that after recall, appearance of the IgG-SCs within the spleen of immunized mice was fast (<24 h) and this early response was free of naive IgG-SCs. We further confirmed that our phenotypic analysis of IgG-SCs after recall strongly correlated with the different employed immunization schemes. Additionally, a phenotypic comparison of IgG-SCs presented in the spleen during immunization or after recall revealed similarities but also significant differences. The developed approach introduced a novel (to our knowledge), quantitative, and functional highly resolved alternative to study the quality of immunizations.
Quantitative modeling of the effect of antigen dosage on B-cell affinity distributions in maturating germinal centers
Laboratoire Colloïdes et Matériaux Divisés - Marco Molari, Klaus Eyer, Jean Baudry, Simona Cocco, Rémi Monasson
Nature Protocols - 15 2920–2955 - DOI: 10.7554/eLife.55678 - 2020
Affinity maturation is a complex dynamical process allowing the immune system to generate antibodies capable of recognizing antigens. We introduce a model for the evolution of the distribution of affinities across the antibody population in germinal centers. The model is amenable to detailed mathematical analysis and gives insight on the mechanisms through which antigen availability controls the rate of maturation and the expansion of the antibody population. It is also capable, upon maximum-likelihood inference of the parameters, to reproduce accurately the distributions of affinities of IgG-secreting cells we measure in mice immunized against Tetanus Toxoid under largely varying conditions (antigen dosage, delay between injections). Both model and experiments show that the average population affinity depends non-monotonically on the antigen dosage. We show that combining quantitative modeling and statistical inference is a concrete way to investigate biological processes underlying affinity maturation (such as selection permissiveness), hardly accessible through measurements.
Deep phenotypic characterization of immunization-induced antibacterial IgG repertoires in mice using a single-antibody bioassay
Laboratoire Colloïdes et Matériaux Divisés - Millie Heo, Guilhem Chenon, Carlos Castrillon, Jérôme Bibette, Pierre Bruhns, Andrew D. Griffiths, Jean Baudry & Klaus Eyer
Communications Biology - 614 5337-5342 - https://doi.org/10.1038/s42003-020-01296-3 - 2020
Antibodies with antibacterial activity need to bind to the bacterial surface with affinity, specificity, and sufficient density to induce efficient elimination. To characterize the anti-bacterial antibody repertoire, we developed an in-droplet bioassay with single-antibody resolution. The assay not only allowed us to identify whether the secreted antibodies recognized a bacterial surface antigen, but also to estimate the apparent dissociation constant (KD app) of the interaction and the density of the recognized epitope on the bacteria. Herein, we found substantial differences within the KD app/epitope density profiles in mice immunized with various species of heat-killed bacteria. The experiments further revealed a high cross-reactivity of the secreted IgG repertoires, binding to even unrelated bacteria with high affinity. This application confirmed the ability to quantify the anti-bacterial antibody repertoire and the utility of the developed bioassay to study the interplay between bacteria and the humoral response.

Apollonian packing in polydisperse emulsions
Laboratoire Colloïdes et Matériaux Divisés - Sylvie Kwok, Robert Botet, Lewis Sharpnack and Bernard Cabane
Nature Protocols - 16 2426-2430 - https://doi.org/10.1039/C9SM01772K - 2020
We have discovered the existence of polydisperse high internal-phase-ratio emulsions (HIPE) in which the internal-phase droplets, present at 95% volume fraction, remain spherical and organise themselves according to Apollonian packing rules. These polydisperse HIPEs are formed by emulsifying oil dropwise in a surfactant-poor aqueous continuous phase. After stirring has ceased, their droplet size distributions begin to evolve spontaneously and continuously through coalescence towards well-defined power laws with the Apollonian exponent. Small-angle X-ray Scattering performed on aged HIPEs demonstrate that the droplet packing structure agrees with that of a numerically simulated random Apollonian packing. We argue that when such concentrated emulsions are allowed to evolve, the coalescing droplets must obey volume and sphericity conservation. This leads to a mechanism that differs from typical coalescence in dilute emulsions.

Swelling, dewetting and breakup in thin polymer films for cultural heritage
Laboratoire Colloïdes et Matériaux Divisés - Amélie Castel, Philipp Gutfreund, Bernard Cabaned and Yahya Rharbi
Soft Matter - 16 1485-1497 - https://doi.org/10.1039/C9SM01976F - 2020
The removal of ultrathin amorphous polymer films in contact with nonsolvent/solvent binary mixtures is addressed by means of neutron reflectometry and atomic force microscopy. The high resolution of neutron scattering makes it possible to resolve the distribution profiles of heavy water and benzyl alcohol inside Laropal®A81, often employed as a protective varnish layer for Culture Heritage in restoration of easel paintings. The swelling kinetics and distribution profiles were recorded as a function of time and increasing benzyl alcohol concentration in water. The varnish film swells by penetration of the good solvent. At higher concentrations water-filled cavities appear inside the varnish and grow with time. Contrary to homogeneous dissolution dewetting is observed at late stages of exposure to the liquid which leads to the Breakup of the film. The high resolution measurements are compared to bulk behaviour characterized by the ternary phase diagram and the Flory–Huggins interaction parameters are calculated and used to predict the swelling and solvent partition in the films. Distinct differences of the thin film to bulk behaviour are found. The expectations made previously for the behaviour of solvent/non-solvent mixtures on the removal of thin layers in the restoration of easel paintings should be revised in view of surface interactions.


Optimised hyperbolic microchannels for the mechanical characterisation of bio-particles
Laboratoire Complex Suspensions - Yanan Liu, Konstantinos Zografos, Joana Fidalgo, Charles Duchene, Clement Quintard, Thierry Darnige, Vasco Filipe, Sylvain Huille, Olivia du Roure, Monica S. N. Oliveira and Anke Lindner
Soft Matter - 16 9844 - DOI: 10.1039/d0sm01293a - 2020
The transport of bio-particles in viscous flows exhibits a rich variety of dynamical behaviour, such as
morphological transitions, complex orientation dynamics or deformations. Characterising such complex
behaviour under well controlled flows is key to understanding the microscopic mechanical properties of
biological particles as well as the rheological properties of their suspensions. While generating regions of
simple shear flow in microfluidic devices is relatively straightforward, generating straining flows in which
the strain rate is maintained constant for a sufficiently long time to observe the objects’ morphologic
evolution is far from trivial. In this work, we propose an innovative approach based on optimised design
of microfluidic converging–diverging channels coupled with a microscope-based tracking method to
characterise the dynamic behaviour of individual bio-particles under homogeneous straining flow.
The tracking algorithm, combining a motorised stage and a microscopy imaging system controlled by
external signals, allows us to follow individual bio-particles transported over long-distances with highquality
images. We demonstrate experimentally the ability of the numerically optimised microchannels
to provide linear velocity streamwise gradients along the centreline of the device, allowing for extended
consecutive regions of homogeneous elongation and compression. We selected three test cases (DNA,
actin filaments and protein aggregates) to highlight the ability of our approach for investigating dynamics
of objects with a wide range of sizes, characteristics and behaviours of relevance in the biological world
Meta population structure and the evolutionary transition to multicellularity
Laboratoire de Génétique de l’Evolution - Caroline J. Rose Katrin Hammerschmidt Yuriy Pichugin Paul B. Rainey
First published - 23(9) 1380-1390 - doi.org/10.1111/ele.13570 - 2020
The evolutionary transition to multicellularity has occurred on numerous occasions, but transitions to complex life forms are rare. Here, using experimental bacterial populations as proxies for nascent multicellular organisms, we manipulate ecological factors shaping the evolution of groups. Groups were propagated under regimes requiring reproduction via a life cycle replete with developmental and dispersal (propagule) phases, but in one treatment lineages never mixed, whereas in a second treatment, cells from different lineages experienced intense competition during the dispersal phase. The latter treatment favoured traits promoting cell growth at the expense of traits underlying group fitness – a finding that is supported by results from a mathematical model. Our results show that the transition to multicellularity benefits from ecological conditions that maintain discreteness not just of the group (soma) phase, but also of the dispersal (germline) phase.

Genotypic and phenotypic analyses reveal distinct population structures and ecotypes for sugar beet‐associated Pseudomonas in Oxford and Auckland
Laboratoire de Génétique de l’Evolution - Xue‐Xian Zhang,corresponding author, Stephen R. Ritchie, Hao Chang, Dawn L. Arnold, Robert W. Jackson, and Paul B. Rainey
Ecol Evol - 10(12) 5963–5975 - doi: 10.1002/ece3.6334 - 2020
Fluorescent pseudomonads represent one of the largest groups of bacteria inhabiting the surfaces of plants, but their genetic composition in planta is poorly understood. Here, we examined the population structure and diversity of fluorescent pseudomonads isolated from sugar beet grown at two geographic locations (Oxford, United Kingdom and Auckland, New Zealand). To seek evidence for niche adaptation, bacteria were sampled from three types of leaves (immature, mature, and senescent) and then characterized using a combination of genotypic and phenotypic analysis. We first performed multilocus sequence analysis (MLSA) of three housekeeping genes (gapA, gltA, and acnB) in a total of 152 isolates (96 from Oxford, 56 from Auckland). The concatenated sequences were grouped into 81 sequence types and 22 distinct operational taxonomic units (OTUs). Significant levels of recombination were detected, particularly for the Oxford isolates (rate of recombination to mutation (r/m) = 5.23 for the whole population). Subsequent ancestral analysis performed in STRUCTURE found evidence of six ancestral populations, and their distributions significantly differed between Oxford and Auckland. Next, their ability to grow on 95 carbon sources was assessed using the Biolog™ GN2 microtiter plates. A distance matrix was generated from the raw growth data (A 660) and subjected to multidimensional scaling (MDS) analysis. There was a significant correlation between substrate utilization profiles and MLSA genotypes. Both phenotypic and genotypic analyses indicated presence of a geographic structure for strains from Oxford and Auckland. Significant differences were also detected for MLSA genotypes between strains isolated from immature versus mature/senescent leaves. The fluorescent pseudomonads thus showed an ecotypic population structure, suggestive of adaptation to both geographic conditions and local plant niches.


METHOD FOR MANIPULATING THE EVOLUTION OF COLLECTIVES OF SELF-REPLICATING ENTITIES AND VARIATION BETWEEN COLLECTIVES OF SELF-REPLICATING ENTITIES
Laboratoire de Génétique de l’Evolution - Paul RAINEY Jérôme BIBETTE Jean BAUDRY Nicolas BREMOND Laurent BOITARD Jairo GARNICA Denis COTTINET
My Science Work - - - 2020
The present invention relates to a method for manipulating the evolution of collectives of self-replicating entities and/or variation between collectives of self-replicating entities, in a high throughput droplet milli-fluidic system.
Experimental manipulation of selfish genetic elements links genes to microbial community function
Laboratoire de Génétique de l’Evolution - Steven D. Quistad, Guilhem Doulcier and Paul B. Rainey
Philosophical Transactions of the Royal Society - - doi.org/10.1098/rstb.2019.0681 - 2020
Microbial communities underpin the Earth's biological and geochemical processes, but their complexity hampers understanding. Motivated by the challenge of diversity and the need to forge ways of capturing dynamical behaviour connecting genes to function, biologically independent experimental communities comprising hundreds of microbial genera were established from garden compost and propagated on nitrogen-limited minimal medium with cellulose (paper) as sole carbon source. After 1 year of bi-weekly transfer, communities retained hundreds of genera. To connect genes to function, we used a simple experimental manipulation that involved the periodic collection of selfish genetic elements (SGEs) from separate communities, followed by pooling and redistribution across communities. The treatment was predicted to promote amplification and dissemination of SGEs and thus horizontal gene transfer. Confirmation came from comparative metagenomics, which showed the substantive movement of ecologically significant genes whose dynamic across space and time could be followed. Enrichment of genes implicated in nitrogen metabolism, and particularly ammonification, prompted biochemical assays that revealed a measurable impact on community function. Our simple experimental strategy offers a conceptually new approach for unravelling dynamical processes affecting microbial community function.



Toward a dynamical understanding of microbial communities
Laboratoire de Génétique de l’Evolution - Paul B. Rainey and Steven D. Quistad
Philosophical Transactions of the Royal Society - - doi.org/10.1098/rstb.2019.0248 - 2020
The challenge of moving beyond descriptions of microbial community composition to the point where understanding underlying eco-evolutionary dynamics emerges is daunting. While it is tempting to simplify through use of model communities composed of a small number of types, there is a risk that such strategies fail to capture processes that might be specific and intrinsic to complexity of the community itself. Here, we describe approaches that embrace this complexity and show that, in combination with metagenomic strategies, dynamical insight is increasingly possible. Arising from these studies is mounting evidence of rapid eco-evolutionary change among lineages and a sense that processes, particularly those mediated by horizontal gene transfer, not only are integral to system function, but are central to long-term persistence. That such dynamic, systems-level insight is now possible, means that the study and manipulation of microbial communities can move to new levels of inquiry.




Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity
Laboratoire de Génétique de l’Evolution - Guilhem Doulcier, Amaury Lambert, Silvia De Monte, Paul B Rainey
EcologyEvolutionary Biology - - DOI: 10.7554/eLife.53433 - 2020
Interactions among microbial cells can generate new chemistries and functions, but exploitation requires establishment of communities that reliably recapitulate community-level phenotypes. Using mechanistic mathematical models, we show how simple manipulations to population structure can exogenously impose Darwinian-like properties on communities. Such scaffolding causes communities to participate directly in the process of evolution by natural selection and drives the evolution of cell-level interactions to the point where, despite underlying stochasticity, derived communities give rise to offspring communities that faithfully re-establish parental phenotype. The mechanism is akin to a developmental process (developmental correction) that arises from density-dependent interactions among cells. Knowledge of ecological factors affecting evolution of developmental correction has implications for understanding the evolutionary origin of major egalitarian transitions, symbioses, and for top-down engineering of microbial communities.





Ecological scaffolding and the evolution of individuality
Laboratoire de Génétique de l’Evolution - Andrew J. Black, Pierrick Bourrat & Paul B. Rainey
Nature Ecology & Evolution - 4 426–436 - doi.org/10.1038/s41559-019-1086-9 - 2020
Evolutionary transitions in individuality are central to the emergence of biological complexity. Recent experiments provide glimpses of processes underpinning the transition from single cells to multicellular life and draw attention to the critical role of ecology. Here, we emphasize this ecological dimension and argue that its current absence from theoretical frameworks hampers development of general explanatory solutions. Using mechanistic mathematical models, we show how a minimal ecological structure comprising patchily distributed resources and between-patch dispersal can scaffold Darwinian-like properties on collectives of cells. This scaffolding causes cells to participate directly in the process of evolution by natural selection as if they were members of multicellular collectives, with collectives participating in a death–birth process arising from the interplay between the timing of dispersal events and the rate of resource use by cells. When this timescale is sufficiently long and new collectives are founded by single cells, collectives experience conditions that favour evolution of a reproductive division of labour. Together our simple model makes explicit key events in the major evolutionary transition to multicellularity. It also makes predictions concerning the life history of certain pathogens and serves as an ecological recipe for experimental realization of evolutionary transitions.







638 publications.