Thematic Session on Reticulate Evolution Before and After the Modern Synthesis: Historical and Epistemological Perspectives and Wider Applications Beyond Traditional Fields
Organized by Nathalie Gontier & Jan Sapp
Eric Bapteste (Department of Systematics, Adaptation and Evolution, Pierre and Joseph Curie University - Paris 6, FR); Francisco Carrapiço (Centre for Ecology, Evolution and Environmental Interaction; Centre for Philosophy of Science, Faculty of Science, University of Lisbon, PT); Luís Correia & António Manso (Laboratory of Agent Modelling (LabMAg), Department of Informatics, University of Lisbon, PT); Ricardo Guerrero & Mercedes Berlanga (Department of Microbiology, University of Barcelona, SP); Élio Sucena & Vitor Faria (Gulbenkian Institute of Science, PT); Davide Vecchi (Centre for Philosophy of Science, University of Lisbon, PT; Laura Weyrich (Australian Centre for Ancient DNA, University of Adelaide, AUS)
Studies of symbiosis, symbiogenesis and lateral gene transfer challenge the Modern Synthesis’ one-genome: one-organism conception. Evidence of reticulate evolution today demands that what counts as an “individual” be reconsidered, and impacts phylogenetic reconstructions of life’s major taxa. New units of evolution have been proposed, including the “holobiont” or “symbiome,” and it is becoming clear that reticulate evolution causally influences processes of speciation as well as extinction. Research on reticulate evolution is also integrated in fields that surpass classic evolutionary biology. Medicine, agriculture, and even the sociocultural sciences (including sociology, anthropology and linguistics) are applying key concepts and methodologies associated with research on symbiosis, symbiogenesis and lateral gene transfer. In this symposium, we bring together historians, philosophers, biologists and anthropologists to discuss 1) the historical roots of symbiosis and its eclectic development in various biological and sociocultural specialties from the 19th century to the present; 2) the epistemic challenges that reticulate evolution presents in providing new mechanisms, units and levels of evolution as well as new iconographies to reconstruct life’s history; and 3) the potential reticulate evolution has to go beyond the biological sciences to model and conceptualize sociocultural evolution.
The small size, ubiquity, metabolic versatility and genetic plasticity of microorganisms allow them to quickly adapt to unfavorable and/or changing environmental conditions. Bacteria and archaea live in complex multispecies communities. Living organisms constantly interact with their habitats, selectively taking up compounds from their surroundings and excreting metabolic products and thus modifying their environment. The consumption of resources and the formation of metabolic products by spatially separated microbial populations constitute the driving force that leads to gradient formation. By the cell theory, the cellular membrane is the first and significant gradient, that differentiates the "I" from the "Other". It has been suggested that communication and cooperation, both within and among bacterial species, have produced emergent properties that give a selective advantage. Bacteria do not function as individuals; rather, the vast majority of bacteria in natural and pathogenic ecosystems live in aggregates referred to as biofilms. These bacterial surface-associated communities are attached to solid substrata. Such metabolically integrated consortia consisting of multiple species can adopt specific spatial configurations. Indeed, the bacterial consortia of biofilms reach levels of complexity nearing those of multicellular eukaryotes. Microbial consortia functions were maintained throughout the evolution, from the first ecosystems, such as microbial mats, to the recently (geologically speaking) intestinal tract of animals, such as the xylophagous insects. The autopoietic unit, whether a cellular biont (minimal autopoietic unit) or a holobiont (integrated biont organisms, i.e., animals or plants, with all of their associated microbiota), is capable of self-maintenance by sensing the environment and is able to adapt and evolve. Complex autopoietic units acquire novel properties when the assembly of their components results in higher functional-structural complexity. However, autopoiesis alone, is a necessary but not a sufficient condition for the evolution of life.
Eric Bapteste - Network-thinking: a complementary perspective to address the compelling epistemological and biological challenges raised by reticulate evolution
Biological objects (from genes to genomes and holobionts) are composite entities, made of interacting heterogeneous parts; often brought together by reticulate processes. Describing the evolution of such complex objects, in particular the association, stabilisation, and transformation of biological elements resulting in novel higher level structures requires the developments of network-based analytical tools and of increasingly flexible representations of life's history. In order to reach this conclusion, I will introduce some conceptual challenges raised by biological data and recent discoveries from microbiology and virology, and explain how these challenges encourage to expand the framework of evolutionary analyses through the use of sequence similarity networks and bipartite graphs.
Francisco Carrapiço - The symbiogenic superorganism concept: An old problem for the neo-Darwinian synthesis?
The concept of superorganic evolution was first introduced into the scientific literature by Herbert Spencer in 1876. Although the term 'superorganism' was not used explicitly, this would imply a new approach to the classical concept of organism. In 1911, William Morton Wheeler, compared the ant society to an organism when observing the biology and social behavior of these insects in colonies. However, it was only in 1928 that he referred to the ant colony as a superorganism. Based on these ideas and further works, we have introduced the concept of symbiogenic superorganism applied to new entities or consortia formed by the integration of individual organisms. This concept includes four main principles: 1. it is composed of different species of organisms living together, which work towards a common goal; 2. the new entity is a polygenomic one, in which the different genomes operate together in a complementary and synergistic way for the whole; 3. the parts and units of this entity modify themselves qualitatively, compared to the same units when isolated; 4. the final outcome of the synergy is not the mere qualitative and/or quantitative sum of the units, which constitute the consortium, acquiring new collective synergies and characteristics. This reality is widespread in nature and well exemplified by Azolla, an aquatic pteridophyte constituted by the association of two type of prokaryote organisms (cyanobacterium and bacteria) living symbiotically inside the leaf cavity of the fern (host). All these facts challenge the traditional neo-Darwinian approach to understanding the organism concept, reinforce the principle that eukaryotes are not entities genetically unique and that the individual must be seen as a complex biological ecosystem, composed of multiple interdependent parts living symbiotically. This new perspective allows for a better understanding of the web of life in our planet and beyond.
Laura Weyrich (Keith Dobney, and Alan Cooper) - Untangling the evolutionary history of the human microbiome using Neandertal dental calculus: Cultural and Environmental Impacts on human health, disease, and evolution
Interpreting the evolutionary history of bacterial communities within the human body (microbiome) is key to understanding multiple aspects of health and disease, and elucidating mechanisms that underlie bacterial and human co-evolution. Although research once suggested that the human microbiome evolved in accordance with the hominid evolutionary tree, recent evidence has indicated that the human microbiome underwent significant changes after the split between human and chimpanzee lineages. To examine this theory in greater detail, we recovered ancient bacterial DNA within dental calculus (calcified dental plaque) from Neandertals, ancient and present-day humans, and greater apes to determine the evolutionary history of the hominid microbiome. Similar bacterial community structures were detected in all non-agriculturalist specimens (Neandertals, chimpanzees, African and European hunter-gatherers), revealing the existence of a once shared hominid microbiome. In contract, a marked change was observed in the oral microbiome when humans adopted agriculture in both Europe and Africa; individuals from both continents exhibited similar core and highly abundant bacterial species, despite the vastly different cultivars and timing. Further alterations to the human oral microbiome were observed after the Industrial Revolution, and again during the coming of the modern age, revealing additional cultural and environmental factors that can significantly impact the human microbiome, and alter the evolutionary signal associated between bacteria and humans. Consequently, essentially all present-day humans possess an evolutionarily recent oral microbiome that was introduced after the introduction of farming Europe, nearly 7,500 years ago. These ancient and historical samples providing timing and reveal cultural and environmental factors that altered the relationship between humans and their microorganisms, which may have significant health consequences in the modern world.
Bacteria of the genus Wolbachia are intracellular symbionts of many animal species. In Drosophila, Wolbachia has been shown to confer protection to RNA virus infection in a strain-dependent manner. Through experimental evolution, we have selected an outbred Wolbachia-infected population of D. melanogaster for increased resistance to DCV, a natural viral pathogen. Whole-genome sequencing of this population, upon 20 generations of selection, revealed that a Wolbachia sub-strain was fixed. Moreover, we show that challenged inter-population hybrids carrying either Wolbachia variant differ in their fitness, confirming the adaptive value to the host of selected endosymbiont. Finally, we re-assess host genome evolution upon Wolbachia clearance and DCV infection over 20 more generations. These findings demonstrate that the presence of protective endosymbiont plays a role in shaping the host genome and its own evolution may have a profound effect on host adaptation.
This talk presents Symbiogenetic MuGA (SMuGA), an integration of symbiogenesis with the Multiset Genetic Algorithm (MuGA) to solve large binary difficult problems. The co-evolutionary model used in SMuGA evolves two species: hosts that represent a solution to the problem, and parasites that represent part-solutions. The novelty of the approach is the varying length of parasites along the evolutionary process. Additionally, it also allows multiple parasites to collaborate with a single host. To improve efficiency, we introduced proxy evaluation of parasites, which saves fitness function calls and exponentially reduces the symbiotic collaborations produced. Another novel feature consists of breaking the evolutionary cycle into two phases: a symbiotic phase and a phase of independent evolution of both hosts and parasites. SMuGA was tested in optimization of a variety of deceptive functions, with results one order of magnitude better than state of the art symbiotic algorithms. This allowed to optimize deceptive problems with large sizes, and showed a linear scaling in the number of iterations to attain the optimum in problems where some decomposition is possible. Future developments of SMuGA include the definition of new genetic operators that operate in parasites and the introduction of mechanisms to preserve genetic diversity of the parasite population. With those improvements we foresee the increased ability of SMuGA to optimize problems with very large genomes and the application of the model to other types of functions.
Davide Vecchi - A symbiotic account of biological individuality
Matter is organised hierarchically, with components creating higher level entities in a recursive way. Herbert Spencer proposed that evolution can be characterized by two principles: continuous multiplication of parts (i.e., instability of the homogeneous) and progressive integration (i.e., stability of the heterogeneous). Living matter is no exception. Teilhard de Chardin considered "conjugation" (i.e., the merging of lineages) and association (i.e., symbiosis) as "elemental movements of life". Whether accidental or not, many evolutionary transitions were the result of processes of integration, most assuredly eukaryogenesis, but possibly also the emergence of cells. So, assuming that symbiosis is an evolutionarily significant process, what does the fact of symbiosis imply for the notion of biological individual? Symbiosis can be characterised as an aggregative force whereby physiologically and reproductively autonomous biological individuals progressively associate by sharing, for example, a metabolic fate. The strength of the association varies from a partial, reversible and transitory association to an obligate, irreversible and permanent one. The strength of the association is inversely proportional to the degree of autonomy of the biological individuals involved. Symbiosis therefore poses a potential problem for those accounts of biological individuality that are based on a static characterisation of autonomy. In fact, the existence of various degrees of physiological and reproductive integration implies the relinquishment of biological autonomy on the part of the host and symbiont. In this talk I will show in what sense the connected concepts of autonomy, autopoiesis and organisational closure are challenged by evidence for symbiosis. The fact of symbiosis demonstrates the interpenetration between living system and environment as well as the ontogenetic and phylogenetic negotiability of their relationship. The fact of symbiosis implies that transitional individuals, mutualistic symbioses and the creation of holobionts are common and evolutionarily significant biological phenomena. But are they?
Reticulate Evolution: Symbiogenesis, Lateral Gene Transfer, Hybridization, and Infectious Heredity, Springer (Dordrecht) 2015, edited by Nathalie Gontier
We kindly invite the symposium participants to a glass of Port to celebrate the publication of the book!
From the cover: Written for non-experts, this volume introduces the mechanisms that underlie reticulate evolution. Chapters are either accompanied with glossaries that explain new terminology or timelines that position pioneering scholars and their major discoveries in their historical contexts. The contributing authors outline the history and original context of discovery of symbiosis, symbiogenesis, lateral gene transfer, hybridization or divergence with gene flow, and infectious heredity. By applying key insights from the areas of molecular (phylo)genetics, microbiology, virology, ecology, systematics, immunology, epidemiology and computational science, they demonstrate how reticulate evolution impacts successful survival, fitness and speciation. Reticulate evolution brings forth a challenge to the standard Neo-Darwinian framework, which defines life as the outcome of bifurcation and ramification patterns brought forth by the vertical mechanism of natural selection. Reticulate evolution puts forward a pattern in the tree of life that is characterized by horizontal mergings and lineage crossings, making the "tree of life" look more like a "web of life." On an epistemological level, the various means by which hereditary material can be transferred horizontally challenges our classic notions of units and levels of evolution, fitness, modes of transmission, linearity, communities, and biological individuality.
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