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VI. Earth Life Emergence: Development of Body, Brain, Selves and Societies

4. Cellular Holobiont Symbiogenesis

Embley, T. Martin and William Martin. Eukaryotic Evolution, Changes and Challenges. Nature. 440/623, 2006. Paired in this issue with the Gavin article below, an update on the role of mitochondrial organelles in the prokaryote to eukaryote transition. But again proteins are said to interact as “machinery,” so an inappropriate natural matrix persists.

Mitochondria in previously unknown biochemical manifestations seem to be universal among eukaryotes, modifying our views about the nature of the earliest eukaryotic cells and testifying to the importance of endosymbiosis in eukaryotic evolution. (623)

Feijen, Frida, et al. Evolutionary Dynamics of Mycorrhizal Symbiosis in Land Plant Diversification. Nature Scientific Reports. 8/10698, 2018. Now that such mutual floral and faunal assemblies, which were long ignored or denied, have become well accepted, Swiss and Dutch botanists can describe their vital presence and contribution to life’s developmental course. See also Unity in Diversity: Ancient Partnerships between Plants and Fungi by K. Field and S. Pressel in New Phytologist (Online April 2108).

Now that such mutual floral and faunal assemblies, which were long ignored or denied, have become well accepted, Swiss and Dutch botanists can describe their vital presence and contribution to life’s developmental course. See also Unity in Diversity: Ancient Partnerships between Plants and Fungi by K. Field and S. Pressel in New Phytologist (Online April 2108).

Frank, Steven. The Origin of Symbiotic Symbiosis. Journal of Theoretical Biology. 176/403, 1995. A review of a new integrative model to explain the evolution of mutually beneficial assemblies.

A dominant theme in the history of life has been the evolutionary innovations of cooperative symbioses: the first genomes near the origin of life, integrated prokaryotic cells, the complex symbiotic communities that evolved into modern eukaryotic cells, lichens, mycorrhizae, and so on. (403)

Gavin, Anne-Claude, et al. Proteome Survey Reveals Modularity of the Yeast Cell Machinery. Nature. 440/631, 2006. An exemplary article with 32 authors from across Europe, worth several comments. With prokaryotic and eukaryotic cellular components now identified, the dynamic interrelations between them can be recognized. This approach reveals constant information-based, “cross-talk” processes whence similar modular encapsulation repeats over and over. A universality is here implied but a machine metaphor remains in use throughout. Scientists seem to proceed, mostly unbeknownst and to their disservice, within a physical universe conceived as a material mechanism, whereof life and mind is an interloper.

We first derived a ‘socio-affinity’ index that quantifies the propensity of proteins to form partnerships. (632) The degree of core-module cross-talk between functional categories highlights many known connections, such as that between protein synthesis, transcription and the cell cycle, in addition to others less well established. (634)
The (proteome) modularity is highly reminiscent of that seen elsewhere in nature, for example the combinatorial use of amino acids to build polypeptides, or domains to create proteins with complex biochemical properties. Modularity might very well represent a general attribute of living matter, with de novo invention being rare and reuse the norm. (635)

Gerardo, Nicole. Harnessing Evolution to Elucidate the Consequences of Symbiosis. PLoS Biology. Online February, 2015. A commentary by the Emory University biologist on the article Mutualism Breakdown by Amplification of Wolbachia Genes in the same issue by Ewa Chrostek and Luis Teixeira. We note for the contribution, and to show how symbiotic activities are now caccepted as the common rule, which the late Lynn Margulis valiantly advocated for decades.

Many organisms harbor microbial associates that have profound impacts on host traits. The phenotypic effect of symbionts on their hosts may include changes in development, reproduction, longevity, and defense against natural enemies. Determining the consequences of associating with a microbial symbiont requires experimental comparison of hosts with and without symbionts. Then, determining the mechanism by which symbionts alter these phenotypes can involve genomic, genetic, and evolutionary approaches; however, many host-associated symbionts are not amenable to genetic approaches that require cultivation of the microbe outside the host. In the current issue of PLOS Biology, Chrostek and Teixeira highlight an elegant approach to studying functional mechanisms of symbiont-conferred traits. They used directed experimental evolution to select for strains of Wolbachia wMelPop (a bacterial symbiont of fruit flies) that differed in copy number of a region of the genome suspected to underlie virulence. Their study highlights the power of exploiting alternative approaches when elucidating the functional impacts of symbiotic associations. (Abstract)

Geva-Zatorsky, Naama, et al. When Cultures Meet: The Landscape of “Social” Interactions between the Host and Its Indigenous Microbes. BioEssays. Online August, 2019. As this composite organism model gains use acceptance, with some resistance, N G-Z, Technicon-Israel Institute of Technology, with Eran Elinav and Sven Pettersson, Canadian Institute for Advanced Research, Toronto, provide a comparative sociological and cultural dimension. To paraphrase, we contain multitudes which in turn make up our integral persona, which is here cleverly enhanced and expanded to health, psychological, and urbane realms.

Animals exist as biodiverse composite organisms that include microbes, eukaryotic cells, and organs. Through an interdependent relationship and an inherent ability to transmit and reciprocate stimuli in a bidirectional way, a human body, aka holobiont, secures growth, health, and reproduction. In this review an overview is provided on the communications between microbes and their host in mutually nurturing biochemical, biological, and social interconnected relationships.. Nutrition, immunology, and sexual dimorphism have been traversed extensively to reflect on health and mind states, social interactions, and urbanization defects/effects. Finally, examples of molecular mechanisms potentially orchestrating these complex trans-kingdom interactions are provided. (Abstract excerpt)

Gilbert, Scott and Alfred Tauber. Rethinking Individuality: The Dialectics of the Holobiont. Biology & Philosophy. Online October, 2016. A Swarthmore College biologist and a Boston University philosopher (search each) continue their consideration of organisms, and human beings, as communal mutualities by way of populations of microbial entities. This entry views the immune system as a prime instance, aided by “the recent recognition of the ubiquity of symbiosis.” But concurrent articles in this journal such as Holobionts and the Ecology of Organisms: Multi-species Communities or Integrated Individuals? By Derek Skillings, and An Exploration of Holobiosis and Evolutionary Theory by Ford Doolittle and Austin Booth have quandaries and offer revisions.

However, this autonomous notion of individuality has proven inadequate both in terms of current understanding of organismic organization and more specifically in regards to immune functions in various capacities beyond its defensive role. Beyond the difficulties of defining the individual immunologically, the recent surge of interest in immune processes mediating mutualistic relationships has further challenged the notion of immune mediated individuality (under the guise of the ‘immune self’). Following this line of criticism, the challenge of reconsidering immunology’s guiding precepts is that most (if not all) ‘‘individual’’ animals are increasingly appreciated as being organized consortia of hundreds of species living in a symbiotic commune. What had been previously described as ‘‘individual organisms’’ are, in fact, multi-species/multi-lineage ‘‘holobionts,’’ composite organisms, whose physiology is a co-metabolism between the host and its microbiome, whose development is predicated upon signals derived from these commensal microorganisms, whose phenotype is predicated on microbial as well as host genes, and whose immune system recognizes these particular microbes as part of its ‘‘self.” (2)

Gilbert, Scott, et al. Eco-Evo-Devo: Developmental Symbiosis and Developmental Plasticity as Evolutionary Agents. Nature Reviews Genetics. 16/10, 2015. Gilbert, Swarthmore College, Thomas Bosch, Christian-Albrechts University, and Cristina Ledon-Rettig, Indiana University, propose an expanded synthesis as mutual symbiotic benefits become evident in every aspect of biology. A “phylosymbiosis” proceeds by a reciprocity of symbiont component and holobiont host, which then recapitulates throughout an evolutionary gestation. By an historical review from Charles Darwin and Karl Mobius to Lynn Margulis, Carl Woese, Nancy Moran, Margaret McFall-Ngal, and others, the revolution has been long in the making. A phenotypic organism thus is a composite of its animal genome, resident symbionts, and an abiotic environment. A succinct 2015 summary with 165 references.

The integration of research from developmental biology and ecology into evolutionary theory has given rise to a relatively new field, ecological evolutionary developmental biology (Eco-Evo-Devo). This field integrates and organizes concepts such as developmental symbiosis, developmental plasticity, genetic accommodation, extragenic inheritance and niche construction. This Review highlights the roles that developmental symbiosis and developmental plasticity have in evolution. Developmental symbiosis can generate particular organs, can produce selectable genetic variation for the entire animal, can provide mechanisms for reproductive isolation, and may have facilitated evolutionary transitions. Developmental plasticity is crucial for generating novel phenotypes, facilitating evolutionary transitions and altered ecosystem dynamics, and promoting adaptive variation through genetic accommodation and niche construction. In emphasizing such non-genomic mechanisms of selectable and heritable variation, Eco-Evo-Devo presents a new layer of evolutionary synthesis.

Giorgi, Franco, et al. The Egg as a Semiotic Gateway to Reproduction. Biosemiotics. Online September, 2013. Giorgi, University of Pisa, Luis Emilio Bruni, Aalborg University, Denmark, and Louis Goldberg, SUNY Buffalo, propose that an “oogenesis” oriented development from egg to I may best be understood by way of information conveyances in dual textually semiotic digital and analog modes.

The egg behaves as a prospective cell sustaining the developmental processes of the future embryo. In biosemiotic terms, this apparent teleonomic behaviour can be accounted for without referring to the exclusive causal role played by its genetic makeup. We envision two different processes that are uniquely found in the oocyte: (1) the first involves the mechanisms by which large amounts of mRNA accumulate in the ooplasm to establish the embryo axes prior to fertilization; (2) the second involves transfer of an excess of maternally supplied ribosomes to the oocyte to provide the future embryo with newly synthesized proteins. In this paper, we argue that the information required to sustain embryonic development is not due to any physical properties of the zygotic DNA and the maternal mRNAs, but to their spatially and temporally ordered relationship in the zygote’s internal space. (Abstract)

The oocyte itself is a topologically closed system since it is a cell bounded by a plasma membrane. The existence of such a boundary makes it possible for the oocyte to build up an internal organized ooplasm with an autoreferential character and to refer to the mother’s body as another entity occupying its external environment. This situation stems directly from the necessity to distinguish the content to be described, and eventually to be constructed as the internal organized structure of the oocyte, from its surroundings: a clear distinction between what could be defined as selfhood and everything else that is to be experienced as otherness. It follows that self-description is a pre-condition for the system to undergo self-replication. Self-description and self-replication are thus two key processes that together allow the oocyte to constitute a new emerging individuality distinct from the mother’s body and to maintain unaltered the species’ heritage from generation to generation. (2)

In conclusion, we have claimed a unique status for the oocyte. The single cell carries within it the digitalized memory of the history of the species in the form of a haploid chromosome set and the analogically organized ooplasm in the form of differentially distributed transcripts. Following fertilization, it is the interaction between the zygotic nuclei and the maternally generated transcripts that allows the developmental potential of the embryo to be fully unfolded, even though the structural organization of the ooplasm involves more than just their topological distribution. Many additional hierarchical levels constrain the context-dependent interpretations on local contingencies, as they gradually unfold from these prime interactions. (7)

Gontier, Nathalie. How Symbiosis, Horizontal Gene Transfer, and Virolution Call for an Extended Synthesis. http://aaas.confex.com/aaas/2013/webprogram/Session5780.html.. An AAAS session at the February 2013 Boston annual meeting, organized by the University of Lisbon philosopher. Speakers include Douglas Zook, “Symbiosis as a Driving Force of Evolution,” Frederic Bouchard “How Research on Symbiosis Should Transform Our Understanding of Adaption,” and Gontier on “Importance of Horizontal Evolution for the Sociocultural Sciences.” See also on this site a parallel session “How Macro-Evolutionary Studies Call for an Extended Synthesis.”

Comparative (meta)genomics have made us realize that horizontal evolutionary phenomena have been vastly underestimated. The serial endosymbiogenetic theory has proven the symbiogenetic origin of mitochondria and plastids. Symbiosis studies further prove that symbiotic unions continue to be relevant to understand evolution. Symbiotic unions can become transmitted vertically, from parent to offspring, through means other than germ-line transmission. Abundant evidence also exists for horizontal or lateral gene transfer in microorganisms. And evidence is piling up that lateral gene transfer also occurs abundantly in eukaryotic organisms. Gene sequencing techniques further prove that viruses also contribute to the evolution of life. They may have played a crucial role in the development of the genetic code, and viral genes are abundantly present in non-coding DNA regions that used to be designated as “junk DNA.” Such horizontal evolutionary phenomena pose major challenges to the Modern Synthesis, which makes a clear distinction between ontogeny and phylogeny, emphasizes germ-line transmission, and defines speciation as a splitting or “branching off” process. Horizontal evolutionary studies have consequences for how we define units of evolution, and biological individuals, how we draw the tree of life, and how we conceptualize speciation. (Session Abstract)

Gontier, Nathalie. Universal Symbiogenesis: An Alternative to Universal Selectionist Accounts of Evolution. Symbiosis. 44/1-3, 2007. A paper presented at the 5th International Symbiosis Society Congress in Vienna by the Vrije Universiteit Brussel research philosopher that begins with a good review of the Darwinian prevalence of selective winnowing alone. But as many writers aver, this view is an inadequate explanation that needs to be complemented and advanced by prior, innate affinities for mutual assembly. Examples are then offered across the strata from prokaryotes and viruses to cultures and languages to reveal how ubiquitous in nature this cooperative “hybridization” effect is. See also Nathalie's chapter Introducing Universal Symbiogenesis in Special Sciences and the Unity of Science, Olga Pombo, et al, eds. (Springer, 2012).

The process of symbiogenesis need not be confined to either the microcosm or the origin of eukaryotic beings. On the contrary, just as natural selection today is being universalized by evolutionary biologists and evolutionary epistemologists, symbiogenesis can be universalized as well. It will be argued that in its universalized form, symbiogenesis can provide: (1) a general tool to examine various forms of interaction between different biological organisms (regular symbiogenesis, hybridization, virus-host interactions), and (2) new metaphors for extra-biological fields such as cosmology, the cultural sciences, and language. Universal symbiogenesis can thus complement universal selectionist accounts of evolution. (167)

Definition: Universal symbiogenesis is the process whereby new entities are introduced because of the interactions between (different) previously independently existing entities. These interactions encompass horizontal mergings and the new entities that emerge because of this are called symbionts. (174-175)

Gontier, Nathalie, ed. Reticulate Evolution. Berlin: Springer, 2015. “Reticulate” is meant to represent nature’s pervasive symbiogenesis by way of networks geometries. A lead chapter is Symbiosis – Evolution’s Co-Author by Douglas Zook, a colleague of the late Lynn Margulis. The University of Lisbon editor goes on to include horizontal gene transfer as another instance. A typical entry is Can We Understand Evolution Without Symbiogenesis? by Francisco Carrapico.

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