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A Sourcebook for the Worldwide Discovery of a Creative Organic Universe
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VI. Earth Life Emergence: Development of Body, Brain, Selves and Societies

5. Multicellular Fauna and Flora Organisms

Ruiz-Trillo, Iraki, et al. The Origins of Multicellularity: a Multi-taxon Genome Initiative. Trends in Genetics. 23/3, 2007. A multi-author paper that lays out the project introduced in the abstract below.

The emergence of multicellular organisms from single-celled ancestors – which occurred several times, independently in different branches of the eukaryotic tree – is one of the most profound evolutionary transitions in the history of life. These events not only radically changed the course of life on Earth but also created new challenges, including the need for cooperation and communication between cells, and the division of labor among different cell types. However, the genetic changes that accompanied the several origins of multicellularity remain elusive. Recently, the National Human Genome Research Institute endorsed a multi-taxon genome-sequencing initiative that aims to gain insights into how multicellularity first evolved. This initiative (which we have termed UNICORN) will generate extensive genomic data from some of the closest extant unicellular relatives of both animals and fungi. (113)

Sachs, Joel and James Bull. Experimental Evolution of Conflict Mediation Between Genomes. Proceedings of the National Academy of Sciences. 102/390, 2005. Transitions to a new level of biological complexity requires cooperation among members, but a selection for individual advantage would seem to thwart that. In this study, an evolutionary life cycle for two bacteriophages inherently produced a salutary balance of interaction and independence. These findings, along with evidence from other stages, infer an innate propensity in emergent nature for cooperative behavior.

Specifically, the two phages evolved to copackage their genomes into one protein coat, ensuring cotransmission with each other and virtually eliminating conflict. (390) Our results parallel a variety of conflict mediation mechanisms existing in nature: evolution of reduced genomes in symbionts, cotransmission of partners, and obligate coexistence between cooperating species. (390)

Schopf, William. Cradle of Life. Princeton: Princeton University Press, 1999. A chatty exposition about Precambrian cellular organisms as “the discovery of earth’s earliest fossils,” with paleontologist Schopf as a major player.

Sebe-Pedros, Arnau, et al. The Origin of Metazoa: A Unicellular Perspective. Nature Reviews Genetics. 18/8, 2017. Not only has multicellularity evolved independently multiple times in eukaryotes, but each of these transitions also occurred at different time in the history of life. (499) Akin to van Gestel and Tarnita 2017, Weizmann Institute of Science, University of Queensland, and University of Barcelona researchers provide a wide and deep study of life’s persistent tendency to evolve into more complex unitary organisms. With an emphasis on a “unicellular urmetazoan genome,” a common cyclical process can be identified that occurs each many times. Figure 5 depicts “the origin of multicellularity as a transition from temporal to spatiotemporal cell differentiation.” Phylogenetic relationships of unicellular Holozoa and animals are then traced from fungi to mammals and we human beings whom collectively (another MET) in retrospect are able to learn all this. Some 150 references are cited in support.

The first animals evolved from an unknown single-celled ancestor in the Precambrian period. Recently, the identification and characterization of the genomic and cellular traits of the protists most closely related to animals have shed light on the origin of animals. Comparisons of animals with these unicellular relatives allow us to reconstruct the first evolutionary steps towards animal multicellularity. Here, we review the results of these investigations and discuss their implications for understanding the earliest stages of animal evolution, including the origin of metazoan genes and genome function. (Abstract)

Simpson, Carl. Adaptation to a Viscous Snowball Earth Ocean as a Path to Complex Multicellularity. American Naturalist. 198.5, 2021. As our collaborative studies proceed to reconstruct past planetary environs from which we all arose, the University of Colorado Museum of Natural History geobiologist (search) presents a thorough scenario of colder, glacial and milder, conducive phases that have affected complex organisms. It again amazes that our sapient issue can turn and retrace such a circuitous, stressful course, which reveals how chancy and perilous it was. See also Reproductive Innovations and Pulsed Rise in Plant Complexity by A. Leslie, C. Simpson and L. Mander in Science (373/1308, 2021).

Animals, fungi, and algae with complex multicellular bodies all evolved independently from unicellular ancestors. The early history of these major eukaryotic multicellular clades co-occur with an extreme phase of global glaciations known as the Snowball Earth. Here, I propose that the long-term loss of low-viscosity environments due to several rounds global glaciation drove the multiple origins of complex multicellularity in eukaryotes and the subsequent radiation of complex multicellular groups into previously unoccupied niches. In this scenario, life adapts to Snowball Earth oceans by evolving larger bodies and faster speeds for high-viscosity seawater. Warm, low-viscosity seawater returned with the melting of the glaciers which gave rise to new vital complexities. (Abstract)

Simpson, Carl. The Evolutionary History of Division of Labour. Proceedings of the Royal Society B. 279/116, 2012. A Duke University biologist contributes to the recognition that living systems at any and all scales evolve and emerge in complexity and cognizance by virtue of a reciprocal diversification of functional roles, as they proceed with a further formation of a bounded, individuated whole.

Functional specialization, or division of labour (DOL), of parts within organisms and colonies is common in most multi-cellular, colonial and social organisms, but it is far from ubiquitous. Several mechanisms have been proposed to explain the evolutionary origins of DOL; the basic feature common to all of them is that functional differences can arise easily. These mechanisms cannot explain the many groups of colonial and social animals that exhibit no DOL despite up to 500 million years of evolution. Here, I propose a new hypothesis, based on a multi-level selection theory, which predicts that a reproductive DOL is required to evolve prior to subsequent functional specialization. I test this hypothesis using a dataset consisting of the type of DOL for living and extinct colonial and social animals. The frequency distribution of DOL and the sequence of its acquisition confirm that reproductive specialization evolves prior to functional specialization. A corollary of this hypothesis is observed in colonial, social and also within multi-cellular organisms; those species without a reproductive DOL have a smaller range of internal variation, in terms of the number of polymorphs or cell types, than species with a reproductive DOL. (Abstract, 116)

Smith, Cameron, et al. Emergence of Self-Reinforcing Information Bottlenecks in Multilevel Selection. arXiv:1506.04611. As the Abstract explains Smith, Albert Einstein College of Medicine, with Matthieu Laneuville and Nicholas Guttenberg, Earth-Life Science Institute, Tokyo, provide more insights into evolution’s persistence to recurrently form into more complex, inclusive, viable organisms. See similar works by Kapheim, Rehan, Van Gestel, and others as this transitions model grows in veracity.

We explain how hierarchical organization of biological systems emerges naturally during evolution, through a transition in the units of individuality. We will show how these transitions are the result of competing selective forces operating at different levels of organization, each level having different units of individuality. Such a transition represents a singular point in the evolutionary process, which we will show corresponds to a phase transition in the way information is encoded, with the formation of self-reinforcing information bottlenecks. We present an abstract model for characterizing these transitions that is quite general, applicable to many different versions of such transitions. As a concrete example, we consider the transition to multicellularity. Specifically, we study a stochastic model where isolated communities of interacting individuals (e.g. cells) undergo a transition to higher-order individuality (e.g. multicellularity). This transition is indicated by the marked decrease in the number of cells utilized to generate new communities from pre-existing ones. In this sense, the community begins to reproduce as a whole via a decreasing number of cells. We show that the fitness barrier to this transition is strongly reduced by horizontal gene transfer. These features capture two of the most prominent aspects of the transition to multicellularity: the evolution of a developmental process and reproduction through a unicellular bottleneck. (Abstract)

Smith, Felisa, et al. Body Size Evolution Across the Geozoic. Annual Review of Earth and Planetary Sciences. 44/523, 2016. A dozen scientists from geologists to paleontologists at American universities including Daniel McShea take a billion year retrospective review of life’s complex anatomy and physiology development across the bacteria, archaea, and eukarya domains. Re the second quote, it is evident that this course indeed concludes with a global humanity whom altogether can reconstruct its ancient heritage.

The Geozoic encompasses the 3.6 Ga interval in Earth history when life has existed. Over this time, life has diversified from exclusively tiny, single-celled organisms to include large, complex multicellular forms. Just how and why this diversification occurred has been a major area of interest for paleontologists and evolutionary biologists for centuries. Here, we compile data on organism size throughout the Geozoic fossil record for the three domains of life. We describe canonical trends in the evolution of body size, synthesize current understanding of the patterns and causal mechanisms at various hierarchical scales, and discuss the biological and geological consequences of variation in organismal size. (Abstract)

Finally, the evolution of large body size has been critical to the development of the geologically most important new group sincy cyanobacteria – humankind. Humans not only alter the biosphere but are now also modifying many global biogechemical cycles. Moreover, humans are among the most important forces moving sediment across continents, with the nutrient runoff from agriculture causing the development of widespread anoxic dead zones in many coastal marine settings. The capacity of humans to take these actions depends upon body size sufficiently large to support a brain sophisticated enough to develop language, use tools, and ultimately develop a complex, technological society. (545)

Sogabe, Shunsuke, et al. Pluripotency and the Origin of Animal Multicellularity. Nature. 570/519, 2019. Nine University of Queensland biologists including Sandie and Bernard Degnan contribute to a revisionary understanding of how organisms got going on their evolutionary way. Instead of a single step via clumped unicells, ancestral ur-cells are seen to differentiate at various stages in a life cycle before actual multicellularity. This effect is conveyed by the term pluripotency for cellular material capable to developing into several forms such as stem cells. See a commentary on this work as Scientists Debate the Origin of Cell Types in the First Animals by Jordana Cepelewicz in Quanta Magazine (Online July 17, 2019).

A widely held but rarely tested hypothesis for the origin of animals is that they evolved from a unicellular ancestor that structurally resembled modern sponge choanocytes and choanoflagellates. Here we test this by comparing the transcriptomes, fates and behaviours of the three primary sponge cell types. Together, these analyses argue against homology of sponge choanocytes and choanoflagellates, and the view that the first multicellular animals were simple balls of cells with limited capacity to differentiate. Instead, our results are consistent with the first animal cell being able to transition between multiple states in a manner similar to modern transdifferentiating and stem cells. (Abstract excerpt)

Sole, Ricard, et al. The Road to Synthetic Multicellularity. Current Opinion in Systems Biology. 7/60, 2018. Universitat Pompeu Fabra, Barcelona, and University of Birmingham, UK scientists scope out a project map which scans the journey so far along with a route ahead to spatial patterns, developmental programs, proto-organisms, embodied evolved multicellularity, and long-term evolution via synthetic ecosystems projects. See also, e.g. Model Microbial Communities for Ecosystems Biology in this journal (6/51, 2017).

Multicellularity is a crucial innovation that has taken place independently at least 25 times in the evolution of life on our planet. Uncovering the evolutionary rules associated to the emergence of this transition has been partially achieved thanks to a combination of comparative cell biology, phylogenetic, palaeobiology and genomic studies of primitive model organisms. An alternative path to this goal is the use of synthetic and systems approximations including both experimental and mathematical models. Here we review several key results, formulate a list of open problems and suggest potentially relevant avenues to follow at the crossroads between ecology, evolution and development. (Abstract)

Trewavas, Anthony. The Green Plant as an Intelligent Organism. Baluska, Frantisek, et al, eds. Communication in Plants. Berlin: Springer, 2006. The University of Edinburgh botanist finds a responsive cognitive capacity across the flora kingdoms similarly distinguished by information processing, learning, decision making, choice, predictive modeling, associative memory, sensory integration, and behavioral control. See also a similar article in Trends in Plant Science for September 2005.

Van Gestel, Jordi and Corina Tarnita. On the Origin of Biological Construction, with a Focus on Multicellularity. Proceedings of the National Academy of Sciences. 114/11018, 2017. As the major evolutionary transitions model (see Section VI.H.8) steadily gains acceptance, akin to Sebe-Pedros 2017, University of Zurich and Princeton University systems biologists and ecologists (search each) add a more detailed explanation of how simpler individual organic forms may proceed to join and merge into complex, aggregate whole units. A generic, common life cycle is specified which contributes a perception of the same, independent pattern of diversity, convergence and emergence at work for each nested stage, as the Abstract alludes. A hundred references are cited in support. So in late 2017, unawares as yet, a genesis synthesis becomes robustly evident.

Biology is marked by a hierarchical organization: all life consists of cells; in some cases, these cells assemble into groups, such as endosymbionts or multicellular organisms; in turn, multicellular organisms sometimes assemble into yet other groups, such as primate societies or ant colonies. The construction of new organizational layers results from hierarchical evolutionary transitions, in which biological units (e.g., cells) form groups that evolve into new units of biological organization (e.g., multicellular organisms). Despite considerable advances, there is no bottom-up, dynamical account of how, starting from the solitary ancestor, the first groups originate and subsequently evolve the organizing principles that qualify them as new units.

Guided by six central questions, we propose an integrative bottom-up approach for studying the dynamics underlying hierarchical evolutionary transitions, which builds on and synthesizes existing knowledge. This approach highlights the crucial role of the ecology and development of the solitary ancestor in the emergence and subsequent evolution of groups, and it stresses the paramount importance of the life cycle: only by evaluating groups in the context of their life cycle can we unravel the evolutionary trajectory of hierarchical transitions. The central research questions outlined here naturally link existing research programs on biological construction (e.g., on cooperation, multilevel selection, self-organization, and development) and thereby help integrate knowledge stemming from diverse fields of biology. (Abstract)

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