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Schematics of four contrasting life cycles each with one or more “unicellular bottlenecks” (indicated by an asterisk). Diploid cells and organisms are shaded; haploid cells and organisms are unshaded. For simplicity, each organism is depicted as a hermaphrodite. (A) The haplobiontic-haploid life cycle in which the multicellular phase develops after zygotic meiosis. (B) The haplobiontic-diploid life cycle in which the multicellular phase develops from zygotic mitosis. (C) The diplobiontic life cycle containing two multicellular individuals, one developing after zygotic mitosis and another developing from meiosis. (D) An asexual life cycle in which the multicellular organism and its unicellular (or cloned) propagules resulting from mitotic cellular division (or fragmentation).
Source publication
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...
Contexts in source publication
Context 1
... reproduction is not required to override the conflict between the individual and its constituent cells (Buss 1987;Michod 1997;Nanjundiah and Sathe 2011). Certainly, in the absence of somatic mutations, the presence of a zygote in any life cycle assures genetic homogeneity by providing a unicellular bottleneck regardless of the type of life cycle (Fig. 2). Likewise, it can be difficult for asexual organisms to escape the consequences of Muller's ratchet (the inevitable accumulation of deleterious mutations). However, asexual multicellular organisms also experience an alignment-of-fitness by means of unicellular or cloned propagules (Fig. ...
Context 2
... bottleneck regardless of the type of life cycle (Fig. 2). Likewise, it can be difficult for asexual organisms to escape the consequences of Muller's ratchet (the inevitable accumulation of deleterious mutations). However, asexual multicellular organisms also experience an alignment-of-fitness by means of unicellular or cloned propagules (Fig. ...
Citations
... The origin of multicellularity is one of the major transitions in evolution [1], arguably the transition that has evolved independently the most, both in prokaryotes [2] and in eukaryotes, at least 25 times [3][4][5][6][7][8][9][10][11][12]. This includes both clonal and aggregative types [5,13]. ...
The emergence of multicellularity is one of the major transitions in evolution that happened multiple times independently. During aggregative multicellularity, genetically potentially unrelated lineages cooperate to form transient multicellular groups. Unlike clonal multicellularity, aggregative multicellular organisms do not rely on kin selection instead other mechanisms maintain cooperation against cheater phenotypes that benefit from cooperators but do not contribute to groups. Spatiality with limited diffusion can facilitate group selection, as interactions among individuals are restricted to local neighbourhoods only. Selection for larger size (e.g. avoiding predation) may facilitate the emergence of aggregation, though it is unknown, whether and how much role such selection played during the evolution of aggregative multicellularity. We have investigated the effect of spatiality and the necessity of predation on the stability of aggregative multicellularity via individual-based modelling on the ecological timescale. We have examined whether aggregation facilitates the survival of cooperators in a temporally heterogeneous environment against cheaters, where only a subset of the population is allowed to periodically colonize a new, resource-rich habitat. Cooperators constitutively produce adhesive molecules to promote aggregation and propagule-formation while cheaters spare this expense to grow faster but cannot aggregate on their own, hence depending on cooperators for long-term survival. We have compared different population-level reproduction modes with and without individual selection (predation) to evaluate the different hypotheses. In a temporally homogeneous environment without propagule-based colonization, cheaters always win. Predation can benefit cooperators, but it is not enough to maintain the necessary cooperator amount in successive dispersals, either randomly or by fragmentation. Aggregation-based propagation however can ensure the adequate ratio of cooperators-to-cheaters in the propagule and is sufficient to do so even without predation. Spatiality combined with temporal heterogeneity helps cooperators via group selection, thus facilitating aggregative multicellularity. External stress selecting for larger size (e.g. predation) may facilitate aggregation, however, according to our results, it is neither necessary nor sufficient for aggregative multicellularity to be maintained when there is effective group-selection.
... The tissues of plants (discussed elsewhere [26,27]), are a unitary 1 According to a past president of the Association for Computing Machinery, opening a 2010 symposium on "What is Computation," "We are discovering that neither we in the field nor our friends outside agree on what this term [computation] means … We need a better answer." He goes on to note that newer formulations, leading to "the computational model of representationtransformation," "refocuses the definition of computation from computers to information processes," but that "information processes can be treacherous territory, because "information" is such an ill-defined and conflicted term, despite many efforts to establish international standards for its definition." ...
... For example, it is common to focus on the "complex" multicellular groups (Knoll 2011) to understand the evolution of multicellularity (Simpson 2011). But there are many other multicellular species and lineages (Bonner 2001;McShea 2001;Costa 2006;McShea and Simpson 2011;Herron et al. 2013;Niklas and Newman 2013) that do not possess germ-soma division of labor yet have much to teach, not just about multicellularity but also about how transitions occur. And engaging with these empirical examples should help untangle the conceptual issues around levels of selection, particularly when a new level of fitness is gained. ...
The fitness of groups is often considered to be the average fitness among constituent members. This assumption has been useful for developing models of multilevel selection, but its uncritical adoption has held back our understanding of how multilevel selection actually works in nature. If group fitness is only equal to mean member fitness, then it is a simple task to erode the importance of group-level selection in all multilevel scenarios—species selection could then be reduced to organismal selection as easily as group selection can. Because selection from different levels can act on a single trait, body size, for example, there must be a way to translate one level of fitness to another. This allows the calculation of the contributions of selection at each level. If high-level fitness is not a simple function of member fitness, then how do they interlace? Here we reintroduce Leigh Van Valen’s argument for the inclusion of expansion as a component of fitness. We show that expansion is an integral part of fitness even if one does not subscribe to the energetic view of fitness from which Van Valen originally derived it. From a hierarchical perspective, expansion is the projection of demographic fitness from one level to the next level up; differential births and deaths at one level produce differential expansion one level above. Including expansion in our conceptual tool kit helps allay concerns about our ability to identify the level of selection using a number of methods as well as allowing for the various forms of multilevel selection to be seen as manifestations of the same basic process.
... Multicellularity evolved many times during the evolutionary history of eukaryotes (Grosberg and Strathmann 2007). In most cases, the emergence of multicellularity from unicellular ancestors produced relatively simple life forms, but in a small number of lineages this transition was followed by an elaborate series of events that gave rise to what can be considered 'complex multicellular' organisms, associated with the evolution of intricate developmental processes (Knoll 2011;Niklas and Newman 2013). The emergence of complex multicellularity is thus thought to be a rare event, having occurred independently in animals, fungi, plants, red and brown algae (Knoll 2011). ...
Complex multicellularity has emerged independently across a few eukaryotic lineages and is often associated with the rise of elaborate, tightly coordinated developmental processes. How multicellularity and development are interconnected in evolution is a major question in biology. The hourglass model of embryonic evolution depicts how developmental processes are conserved during evolution, predicting morphological and molecular divergence in early and late embryo stages, bridged by a conserved mid-embryonic (phylotypic) period linked to the formation of the basic body plan. Initially found in animal embryos, molecular hourglass patterns have recently been proposed for land plants and fungi. However, whether the hourglass pattern is an intrinsic feature of all developmentally complex eukaryotic lineages remains elusive. Here, we tested the prevalence of a (molecular) hourglass in the brown algae, the third most developmentally complex lineage on earth that has evolved multicellularity independently from animals, fungi, and plants. By exploring the evolutionary transcriptome of brown algae with distinct morphological complexities, we uncovered an hourglass pattern during embryogenesis in developmentally complex species. Filamentous algae without a canonical embryogenesis display an evolutionary transcriptome that is most conserved in multicellular stages of the life cycle, whereas unicellular stages are more rapidly evolving. Our findings suggest that transcriptome conservation in brown algae is associated with cell differentiation stages, but not necessarily linked to embryogenesis. Together with previous work in animals, plants and fungi, we provide further evidence for the generality of a developmental hourglass pattern across complex multicellular eukaryotes.
... However, their interpretation as stem groups to animals is a subject of ongoing debate (27,28), as this interpretation strongly relies on the cellular dissimilarities between these fossils and a select few protists, known to be among the closest living relatives of animals. 25 Animals are closely related to choanoflagellates, filastereans, pluriformeans, and ichthyosporeans ( Fig. 1A) (2,(29)(30)(31)(32). These lineages not only partly share a genetic toolkit used by animals for development, but can also form transient multicellular structures and display various temporary cell stages in distinct environments (1,30,33). ...
All animals develop from a single-celled zygote into a complex multicellular organism through a series of precisely orchestrated processes. Despite the remarkable conservation of early embryogenesis across animals, the evolutionary origins of this process remain elusive. By combining time-resolved imaging and transcriptomic profiling, we show that single cells of the ichthyosporean Chromosphaera perkinsii - a close relative that diverged from animals approximately 1 billion years ago - undergo symmetry breaking and develop through cleavage divisions to produce a prolonged multicellular colony with distinct co-existing cell types. Our findings about the autonomous developmental program of C. perkinsii , hint that such animal-like multicellular development is either much older than previously thought or evolved convergently in ichthyosporeans.
One-Sentence Summary
The ichthyosporean C. perkinsii develops via symmetry breaking, cleavage divisions, and forms spatially-organized colonies with distinct cell types.
... Multicellular organisms have greater overall resource requirements than smaller unicellular ones and also a greater likelihood of diffusion limitation of growth (Beardall et al., 2009). Seaweeds have to withstand hydrodynamic forces exerted by moving water and breaking waves, and, unlike phytoplankton, which floats in surface waters, they are attached to the substratum, where light levels can be relatively low (Niklas & Newman, 2013). Here we discuss the evolutionary adaptations of seaweeds to their environment, focusing on resource acquisition (particularly nutrients) and hydrodynamic forces. ...
... [66]. Namely: once in the origin of animalia (metazoa) and amoebozoa, three times in the fungi (for chytrids, ascomycetes, and basidiomycetes), and twice in each of the photosynthetic eukaryotic clades (rhodophytes, stramenopiles, and chlorobionta) [67,68]. ...
In the first description of evolution, the fundamental mechanism is the natural selection favoring the individuals best suited for survival and reproduction (selection at the individual level or classical Darwinian selection). However, this is a very reductive description of natural selection that does not consider or explain a long series of known phenomena, including those in which an individual sacrifices or jeopardizes his life on the basis of genetically determined mechanisms (i.e., phenoptosis). In fact, in addition to (i) selection at the individual level, it is essential to consider other types of natural selection such as those concerning: (ii) kin selection and some related forms of group selection; (iii) the interactions between the innumerable species that constitute a holobiont; (iv) the origin of the eukaryotic cell from prokaryotic organisms; (v) the origin of multicellular eukaryotic organisms from unicellular organisms; (vi) eusociality (e.g., in many species of ants, bees, termites); (vii) selection at the level of single genes, or groups of genes; (viii) the interactions between individuals (or more precisely their holobionts) of the innumerable species that make up an ecosystem. These forms of natural selection, which are all effects and not violations of the classical Darwinian selection, also show how concepts as life, species, individual, and phenoptosis are somewhat not entirely defined and somehow arbitrary. Furthermore, the idea of organisms selected on the basis of their survival and reproduction capabilities is intertwined with that of organisms also selected on the basis of their ability to cooperate and interact, even by losing their lives or their distinct identities.
... En este caso, el origen de la multicelularidad se explica a partir de un organismo ancestral cenocítico que sufrió la celularización, es decir la formación de septos o particiones que condujeron a la formación de una membrana interna alrededor de cada uno de sus núcleos, constituyendo células definidas. Esta propuesta utiliza como evidencia ejemplos de celularización observados en algas xantofitas o en foraminíferos (31,32). ...
El origen de la multicelularidad, y por consecuencia, de la expresión de funciones especializadas en las células que constituyen a un individuo son de gran interés para entender los procesos evolutivos que llevaron al surgimiento de los Metazoarios, de las plantas, de los hongos, así como de otros grupos caracterizados por su organización multicelular en sólo una etapa de su ciclo de vida. Se considera que la multicelularidad tuvo un origen: i) clonal o por división sin separación de las células hijas, ii) por agregación de individuos, iii) por septación de cenocitos o sincicios, o bien fue iv) una respuesta adaptativa a las presiones del medio. De manera adicional, la evidencia derivada de estudios filogenéticos, sumada a la secuenciación de moléculas altamente conservadas durante la Evolución y la comparación entre genomas de organismos de diferentes grupos taxonómicos sugieren que la aparición del estado multicelular fue precedida por el establecimiento de las familias génicas que codifican para las proteínas que componen la maquinaria de señalización y la maquinaria de regulación de la expresión genética en los ancestros unicelulares de los Metazoarios. Estos eventos establecieron el escenario para que apareciera la división de funciones en los primeros organismos multicelulares, y, por ende, la formación de los primeros tejidos con funciones especializadas. En este trabajo hacemos una breve reseña de estos procesos.
... The origin of multicellularity in the evolution of living organisms remains one of the most important discussion topics in evolutionary biology over the past one and a half centuries. The main hypotheses explaining the sequential phylogenetic transformation of colonial protists into the first truly multicellular organisms are well known and discussed many times in specialized scientific and educational literature (see, for example, Zakhvatkin 1949Zakhvatkin , 1956Ivanov 1968;Ivanova-Kazas 1995;Bonner 1998;Grosberg and Stratchmann 2007;Michailov et al. 2009;Knoll 2011;Herron et al. 2013;Niklas and Newman 2013;Suga and Ruiz-Trillo 2013;Umen 2014;Coates et al. 2015;Brunet and King 2017;Malakhov et al. 2019;Colizzi et al. 2020;Lamża 2023, etc.). In these hypotheses and the discussions accompanying them, the main place is given to morpho-anatomical, ontogenetic and molecular changes, without which the transition from the simple unicellular level of life organization to a higher level is impossible. ...
... In addition, there is no clear unequivocal separation of different types of multicellularity. Usually, one speaks only of simple and complex multicellularity (Knoll 2011;Niklas and Newman 2013), implying the presence of differentiated cells and tissues by the latter. However, the degree of differentiation varies greatly from one taxon to another (and even between individual stages of the life cycle of the same species of organisms) and demonstrates numerous chaotic transitions from simpler to more complex options and back. ...
It is demonstrated that the initial method of fertilization in animals (Metazoa), embryophyte plants (Embryophyta), most groups of multicellular oogamous algae, oogamous and pseudoogamous multicellular fungi was internal fertilization (in the broad meaning) in/on the body of a maternal organism. Accordingly, during the bisexual process, the initial method of formation of a daughter multicellular organism in animals was viviparity, and in embryophyte plants and most groups of oogamous multicellular algae – the germination of a zygote in/on the body of maternal organism.
The reproductive criteria of multicellularity are proposed and discussed. In this regard, the multicellularity is considered to subdivide terminologically into three variants: 1) protonemal, the most simple, characteristic of multicellular prokaryotes, most groups of multicellular algae and gametophytes of some higher plants; 2) siphonoseptal, found among multicellular fungi, some groups of green and yellow-green algae; 3) embryogenic, most complicated, known in all animals (Metazoa), all sporophytes and some gametophytes of higher plants (Embryophyta), charophyte green algae Charophyceae s.s., oogamous species of green and brown algae, some genera of red algae.
In addition to the well-known division of reproduction methods into sexual and asexual, it is proposed to divide the reproduction of multicellular organisms into monocytic (the emergence of a new organism from one cell sexually or asexually) and polycytic (fragmentation, longitudinal / transverse division or budding based on many cells of the body of the mother organism), since these two ways have different evolutionary and ontogenetic origins.
... Engineering of multicellular organisms is more difficult because of their extended developmental timelines, which involve intercellular adherence, cell-to-cell and cell-to-environment communication, and cell differentiation (Niklas and Newman 2013). These processes are, in part, coordinated via precisely balanced patterns of gene expression that lead to the appropriate organization and differentiation of cells Satterlee et al. 2020). ...
Key message
Synthetic control systems have led to significant advancement in the study and engineering of unicellular organisms, but it has been challenging to apply these tools to multicellular organisms like plants. The ability to predictably engineer plants will enable the development of novel traits capable of alleviating global problems, such as climate change and food insecurity.
Abstract
Engineering predictable multicellular phenotypes will require the development of synthetic control systems that can precisely regulate how the information encoded in genomes is translated into phenotypes. Many efficient control systems have been developed for unicellular organisms. However, it remains challenging to use such tools to study or engineer multicellular organisms. Plants are a good chassis within which to develop strategies to overcome these challenges, thanks to their capacity to withstand large-scale reprogramming without lethality. Additionally, engineered plants have great potential for solving major societal problems. Here we briefly review the progress of control system development in unicellular organisms, and how that information can be leveraged to characterize control systems in plants. Further, we discuss strategies for developing control systems designed to regulate the expression of transgenes or endogenous loci and generate dosage-dependent or discrete traits. Finally, we discuss the utility that mathematical models of biological processes have for control system deployment.
