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Multicellularity has evolved in several eukaryotic lineages leading to plants, fungi, and animals. Theoretically, in each case, this involved (1) cell-to-cell adhesion with an alignment-of-fitness among cells, (2) cell-to-cell communication, cooperation, and specialization with an export-of-fitness to a multicellular organism, and (3) in some cases, a transition from "simple" to "complex" multicellularity. When mapped onto a matrix of morphologies based on developmental and physical rules for plants, these three phases help to identify a "unicellular ⇒ colonial ⇒ filamentous (unbranched ⇒ branched) ⇒ pseudoparenchymatous ⇒ parenchymatous" morphological transformation series that is consistent with trends observed within each of the three major plant clades. In contrast, a more direct "unicellular ⇒ colonial or siphonous ⇒ parenchymatous" series is observed in fungal and animal lineages. In these contexts, we discuss the roles played by the cooptation, expansion, and subsequent diversification of ancestral genomic toolkits and patterning modules during the evolution of multicellularity. We conclude that the extent to which multicellularity is achieved using the same toolkits and modules (and thus the extent to which multicellularity is homologous among different organisms) differs among clades and even among some closely related lineages.
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... At the roots of this project was the idea that cell differentiation, the traditional distinctive trait of multicellular organisms, could have evolved first within unicellular organisms, contrary to the dominant paradigm (see Figure 1.1) according to which complex multicellular organisms are cell aggregates that later acquired the ability to differentiate into several cell types. This alternate scenario had already been suggested by Ispolatov et al. (2012) and Niklas and Newman (Niklas et al., 2013;Niklas, 2014), and is supported by the ubiquitous presence of the multicellular genetic toolkit among unicellular organisms that are not considered to live in colonies (Rokas, 2008;Ruiz-Trillo et al., 2008;Tikhonenkov et al., 2020). What is more, the widespread existence of non-genetic unicellular heterogeneity 2 (Veening et al., 2008a;Ratcliff et al., 2010;Huh et al., 2011a;Cerulus et al., 2016;Takhaveev et al., 2018) lends further credence to a "differentiation-first" scenario whereby complex multicellular organisms evolved from unicellular ancestors prone to differentiation. ...
... Cell types are self-evident in Animals, Plants and Fungi, the three major clades of multicellular organisms. But multicellularity is pervasive in the tree of Life and seems easily achievable (Niklas et al., 2013), which has even pushed some scientists to diminish the importance of the transition towards multicellularity, making the case for multicellularity as having a status of minor major transition (Grosberg et al., 2007). These cell types can communicate and cooperate; and the evolutionary need for division of labor has actually been claimed to promote differentiation. ...
... In fact, even the basic definition of Multicellularity is subject to longstanding debates, and considerably influences how many clades belong to this category. Regardless of the precise definition of the term, it is clear that Multicellularity arose several times independently in the History of Life (Bonner, 1998b;Niklas et al., 2013;Niklas, 2014) -see Figure 9.1. Under a broad definition based upon aggregative properties, Multicellularity evolved across all domains of Life (Nickell et al., 2003;Bonner, 1998b) -as defined by Woese et al. (1977) and Woese et al. (1990), and since corroborated by Spang et al. (2015) -and, within those domains, among very different and often remote clades like Animals and Plants (Parfrey et al., 2013) or Myxobacteria and Cyanobacteria (Dworkin et al., 1972;Bonner, 1998b). ...
Thesis
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Since Life was born, its tireless evolution has created an exceptional diversity of entities spanning an extravagant range of sizes, from the microscopic molecules underlying heritability and the expression of phenotypes to multicellular organisms and their societies. This great variety of the living world, present both between classes of biological entities and within these classes (e.g. proteins), has often been explained theoretically by assuming the existence of trade-offs – impossibility to optimize multiple traits at once – and / or specific niches as produced by the co-occurrence of multiple nutrients. However, the way in which these internal compromises emerge at the cellular level has remained in general elusive, especially since models of evolution most often overlook the mechanistic foundations and the very functioning of cells. Across this thesis, I try to build mechanistic evolutionary models by studying one of the most fundamental property of living things: how to produce energy, and grow, faster than others? This property is based at the cellular level on the structure and expression of enzymes. Rather than the extreme optimization this role suggests, enzymes have extremely diverse characteristics – some are close to achievable physical limits while others are very far from them – that should be explained. Through a modeling approach of the kinetic processes involved, I have shown that these differences can be explained by different selective contexts, characterizing in particular the reactions in which these enzymes are involved. Furthermore, the expression of an enzyme is the result of a complex selective process involving the obvious interest of catalyzing a given reaction but also overall costs for the cell, both in terms of production of the enzyme and of crowding within the cytoplasm. These constraints can promote the evolution of a selective (partial) expression of a metabolic pathway, leading to the release into the medium of metabolites, which can be used as an energetic source. In turn,this can give rise to the evolution of organisms specialised at these metabolites through a process called cross-feeding. Taking into account these processes in an adaptive dynamic model while also integrating an ecological dimension allowed me to establish the restricted conditions in which the cross-feeding may evolve, shedding light on the preponderant implication of certain metabolites (acetate, glycerol). In a last part, outside the strictly mechanistic framework of the thesis, I develop a model of population genetics intended to clarify the mainsprings of metabolic (weakest link) epistasis and its deleterious consequences on fitness at the mutation-selection-drift equilibrium. Finally, I discuss the perspectives opened up by this whole work, the vocation of which would be to contribute to the development of more realistic genotype- phenotype-fitness maps and to document their quantitative influence on evolution, through the combination of population genetics and systems biology.
... At the broadest level, the evolution of complex multicellularity-the capacity to form three-dimensional structures from differentiated tissue-has enabled the formation of complex reproductive or vegetative structures. Complex multicellularity has likely evolved separately in several fungal phyla, but Pezizomycotina and Agaricomycotina have evolved the most complex structures and appear to represent the earliest origins, as other gains are restricted to individual genera or species-poor clades (Stajich et al. 2009;Knoll 2011;Niklas and Newman 2013;Smith et al. 2013;Nagy 2017;Nagy et al. 2018Nagy et al. , 2020. The size and complexity of multicellular structures are typically of limited extent and restricted to reproductive structures in all putative origins outside of Agaricomycotina and Pezizomycotina. ...
... The size and complexity of multicellular structures are typically of limited extent and restricted to reproductive structures in all putative origins outside of Agaricomycotina and Pezizomycotina. While complex multicellularity may have evolved independently in Taphrinomycotina, this is restricted to three closely related species comprising the genus Neolecta and thus is presumably a more recent evolution of complex multicellularity relative to that in Pezizomycotina, whose late Paleozoic crown node already postdates Silurian-Devonian Protaxites (Stajich et al. 2009;Knoll 2011;Niklas and Newman 2013;Smith et al. 2013;Nguyen et al. 2017;Merényi et al. 2020;Nelsen et al. 2020b). Prototaxites is surely an example of complex multicellularity but one that apparently represented an independent evolution distinct from, and older than, that found in any extant fungal lineage. ...
... The emergence of multicellularity from single-celled life represents a major transition, which has occurred many times independently across the tree of life [1][2][3][4][5][6][7][8]. Multicellularity can arise either by aggregation of single cells that come together or from single cells that are maintained together clonally after division [9][10][11]. ...
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Significant increases in sedimentation rate accompany the evolution of multicellularity. These increases should lead to rapid changes in ecological distribution, thereby affecting the costs and benefits of multicellularity and its likelihood to evolve. However, how genetic and cellular traits control this process, their likelihood of emergence over evolutionary timescales, and the variation in these traits as multicellularity evolves are still poorly understood. Here, using isolates of the ichthyosporean genus Sphaeroforma -close unicellular relatives of animals with brief transient multicellular life stages-we demonstrate that sedimentation rate is a highly variable and evolvable trait affected by at least 2 distinct physical mechanisms. First, we find extensive (>300×) variation in sedimentation rates for different Sphaeroforma species, mainly driven by size and density during the unicellular-to-multicellular life cycle transition. Second, using experimental evolution with sedimentation rate as a focal trait, we readily obtained, for the first time, fast settling and multicellular Sphaeroforma arctica isolates. Quantitative microscopy showed that increased sedimentation rates most often arose by incomplete cellular separation after cell division, leading to clonal “clumping” multicellular variants with increased size and density. Strikingly, density increases also arose by an acceleration of the nuclear doubling time relative to cell size. Similar size- and density-affecting phenotypes were observed in 4 additional species from the Sphaeroforma genus, suggesting that variation in these traits might be widespread in the marine habitat. By resequencing evolved isolates to high genomic coverage, we identified mutations in regulators of cytokinesis, plasma membrane remodeling, and chromatin condensation that may contribute to both clump formation and the increase in the nuclear number-to-volume ratio. Taken together, this study illustrates how extensive cellular control of density and size drive sedimentation rate variation, likely shaping the onset and further evolution of multicellularity.
... Complex multi-cellularity in the eukaryotes is found only where a single-cell life-history bottleneck is also found (Grosberg andStrathmann, 1998, 2007;Bourke, 2011;Fisher et al., 2013). Complex multi-cellularity is not found in cases where multi-cellularity is achieved by cells coming together ( A unicellular bottleneck has arisen once in the animals (Dawkins, 1982;King, 2004), once in the land plants (Ligrone et al., 2012), three times in the fungi (the ascomycetes, basidiomycetes and chytridiomycetes; Niklas and Newman, 2013), once in the red algae (Coelho et al., 2007) and at least once (probably more) in the brown algae (Clayton, 1988;Charrier et al., 2008). For useful reviews, see Grosberg and Strathmann (2007), Bourke (2011, p.13 ...
Thesis
The biological world as we see it today has a part-whole hierarchical structure. For example, eusocial societies are made up of many organisms, multicellular organisms are made up of many cells, those cells contain numerous organelles and so on. This hierarchical organisation is thought to have evolved over a long period of time in a series of events known as ‘evolutionary transitions in individuality’. Evolutionary transitions present an interesting challenge for evolutionary theory because they involve changes in the hierarchical level at which the evolutionary process itself acts. This thesis is intended as a contribution to theoretical work aiming to explain such transitions in the hierarchical structure of life. Evolutionary transitions are extreme cases of the evolution of cooperation. Social evolution theory is the part of evolutionary theory that tries to explain the evolution of cooperation. It typically takes an externalist explanatory stance, explaining cooperative behaviour in terms of external factors (e.g. genetic relatedness) that make cooperation sustainable. In this thesis, I move from an externalist to an interactionist explanatory stance, in the spirit of Lewontin and the niche construction theorists. I develop the theory of social niche construction, which has it that biological entities are both the subject and object of their own social evolution. That is, the niche in which social behaviour occurs is not entirely externally defined but is partly modified by the organisms in it. Then, cooperation and the social niche modifier traits supporting it can each evolve as evolutionary responses to the other. This claim is supported by detailed argument and by simulation modelling. Some important social niche modifiers enabling cooperation (e.g. life-history bottlenecks) have the side-effect of raising the hierarchical level at which the evolutionary process acts. This is because modifier traits acting to align the fitness interests of lower-level units (e.g. cells) in a collective also diminish the extent to which those units are bearers of heritable fitness variance, while augmenting the extent to which collectives of such units (e.g. multicellular organisms) are bearers of heritable fitness variance. So while there is no selection-for evolutionary transitions in individuality, there is selection-of the sufficient conditions for transitions to occur. My explanation for evolutionary transitions is couched only in terms of evolutionary self-interest of the lower-level units, so avoiding many of the problems that befall alternative accounts.
... Cette transition majeure dans l'histoire évolutive des organismes (Buss, 1987;Szathmáry & Maynard Smith, 1995), survenue plusieurs fois indépendamment (Knoll, 2011;Niklas & Newman, 2013), a été permise par l'acquisition de mécanismes de régulation et de maintien de la coopération cellulaire. Les « fondements de la multicellularité » se résument ainsi en cinq mécanismes que sont : (i) l'inhibition de la prolifération, (ii) le contrôle de la mort cellulaire, (iii) la réallocation des ressources, (iv) la division des tâches et (v) la création et le maintien de l'environnement extracellulaire (Aktipis et al., 2015, FIGURE 1). ...
Thesis
Les cancers transmissibles sont des lignées cellulaires malignes qui ont évoluées la capacité de coloniser de nouveaux individus par transmission des cellules cancéreuses elles-mêmes. Considérés comme rares chez les vertébrés, avec seulement une lignée décrite chez le chien et deux chez le diable de Tasmanie, les découvertes depuis 2015 de cinq lignées dans plusieurs espèces de bivalves marins ont remis en question leur rareté dans ce groupe. Ces nouvelles formes parasitaires, qui ne ressemblent à aucune autre entité biologique, posent de nombreuses questions. Chez les bivalves, hormis la description des différentes lignées, peu de données étaient disponibles sur leur biologie, leur écologie et leur évolution. Ma thèse se focalise sur l’étude des cancers transmissibles des moules du genre Mytilus. En combinant plusieurs approches d’écologie, de biologie évolutive et de biologie fonctionnelle, mes travaux ont permis de décrire la distribution et la prévalence de ce cancer dans les populations de moules d’Europe, d’étudier l’histoire évolutive de ces lignées de cancer transmissible, ainsi que d’étudier les réponses des hôtes face à l’invasion par des cellules cancéreuses. Ainsi, nous avons pu montrer (1) que les populations des deux espèces de moules européennes M. edulis et M. galloprovincialis sont touchées par une même et unique lignée de cancer transmissible (MtrBTN2) qui a émergé initialement dans un hôte M. trossulus, qui est également retrouvée chez M. chilensis au Chili et chez M. trossulus en Mer du Japon, et qui est différente de la première lignée décrite initialement dans les populations M. trossulus de Colombie Britannique (MtrBTN1), (2) que la prévalence est globalement faible mais varie selon le fond génétique des hôtes et l’habitat, (3) que le trafic maritime semble créer des passerelles épidémiologiques entre les ports expliquant une plus forte prévalence dans ces habitats anthropisés, (4) que malgré une évolution clonale le MtrBTN2 est polymorphe ce qui suggère une histoire évolutive complexe et possiblement ancienne qui a mené à l’évolution d’au moins deux sous-lignées en Europe, (5) que la dynamique d’invasion intra-hôte par le cancer semble dépendre de l’individu receveur et de l’individu donneur dans le cadre d’infections expérimentales et (6) que cette invasion semble induire chez les individus receveurs une réponse immunitaire majoritairement humorale et un remodelage tissulaire associé à une réponse inflammatoire prolongée. Ces différents résultats permettent aujourd’hui de mieux comprendre la dynamique de ce système hôte-cancer si particulier et ouvrent de nombreuses perspectives. En plus d’être des entités biologiques uniques et intrigantes qui permettent d’étudier le cancer sous un angle évolutif original, les cancers transmissibles sont des modèles biologiques de prédilection pour de nombreuses questions fondamentales de la biologie.
... In addition to the various ecosystems in which chlorophyte algae have settled, the different lineages are also characterized by highly variable morphologies, ranging from motile single cells to sessile multicellular organisms with body plans consisting of multiple tissues (Leliaert et al. 2007). Because of the well-resolved green algal phylogeny, it has been established that the transition from unicellularity to multicellularity took place on multiple independent occasions in both streptophyte and chlorophyte algae (Niklas and Newman 2013;Umen 2014;Del Cortona et al. 2020). Similarly, it is likely that streptophyte algae conquered land multiple times during the course of evolution [reviewed in Delwiche and Cooper (2016) and Fürst-Jansen et al. (2020)], while in the chlorophyte lineage, freshwater to marine transitions (or vice versa) frequently occurred (Dittami et al. 2017). ...
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