Recently, a review regarding the mechanics and evolution of mitochondrial fission appeared in Nature. Surprisingly, it stated authoritatively that the mitochondrial outer membrane, in contrast with the inner membrane of bacterial descent, was acquired from the host, presumably during uptake. However, it has been known for quite some time that this membrane was also derived from the Gram‐negative, alpha‐proteobacterium related precursor of present‐day mitochondria. The zombie idea of the host membrane still surrounding the endosymbiont is not only wrong, but more (...) importantly, might hamper the proper conception of possible scenarios of eukaryogenesis. Why? Because it steers the imagination not only with regard to possible uptake mechanisms, but also regarding what went on before. Here I critically discuss both the evidence for the continuity of the bacterial outer membrane, the reasons for the persistence of the erroneous host membrane hypothesis and the wider implications of these misconceptions for the ideas regarding events occurring during the first steps towards the evolution of the eukaryotes and later major eukaryotic differentiations. I will also highlight some of the latest insights regarding different instances of endosymbiont evolution. (shrink)

The photosynthetic organelle of algae and plants (the plastid) traces its origin to a primary endosymbiotic event in which a previously non‐photosynthetic protist engulfed and enslaved a cyanobacterium. This eukaryote then gave rise to the red, green and glaucophyte algae. However, many algal lineages, such as the chlorophyll c‐containing chromists, have a more complicated evolutionary history involving a secondary endosymbiotic event, in which a protist engulfed an existing eukaryotic alga (in this case, a red alga). Chromists such as diatoms and (...) kelps then rose to great importance in aquatic habitats. Another algal group, the dinoflagellates, has undergone tertiary (engulfment of a secondary plastid) and even quaternary endosymbioses. In this review, we examine algal diversity and show endosymbiosis to be a major force in algal evolution. This area of research has advanced rapidly and long‐standing issues such as the chromalveolate hypothesis and the extent of endosymbiotic gene transfer have recently been clarified. BioEssays 26:50–60, 2004. © 2003 Wiley Periodicals, Inc. (shrink)

A flurry of recent publications have challenged consensus views on the tempo and mode of plastid (chloroplast) evolution in eukaryotes and, more generally, the impact of endosymbiosis in the evolution of the nuclear genome. Endosymbiont‐to‐nucleus gene transfer is an essential component of the transition from endosymbiont to organelle, but the sheer diversity of algal‐derived genes in photosynthetic organisms such as diatoms, as well as the existence of genes of putative plastid ancestry in the nuclear genomes of plastid‐lacking eukaryotes such (...) as ciliates and choanoflagellates, defy simple explanation. Collectively, these papers underscore the power of comparative genomics and, at the same time, reveal how little we know with certainty about the earliest stages of the evolution of photosynthetic eukaryotes. Editor's suggested further reading in BioEssaysEarly steps in plastid evolution: current ideas and controversies AbstractDinoflagellate mitochondrial genomes: stretching the rules of molecular biology Abstract. (shrink)

We group encephalitic behaviors as shown in Table 1. It is striking that the majority of these behaviors, namely groups 1 and 2, help spread viral and bacterial infections underlying encephalitis, a situation similar to Ophiocordyceps unilateralis .Could some of the behaviors in Table 1 be of utility to the host as well? Note that the behavioral symptoms may not coincide with impaired intellect . Furthermore, these symptoms may be vestigial in the sense of having been of utility to the (...) host species at a time when the latter possessed lower intelligence to begin with. It is also important to note that encephalitis is often triggered by physical and emotional stress, so that utility of behaviors is better assessed for such conditions.Continuous and compulsive exploration of one’s environment is of course a recipe for learning and discovery. Drinking, eating, biting, chewi .. (shrink)

Animals and plants can be classified into three distinct groups according to their pH- and pO-values and the ratios of inorganic ion concentrations and organic molecule concentrations in their intracellular or extracellular saps . The origin of these types could be sought in the evolutionary change from aquatic to terrestrial environment. The widespread existence of these types in nature enables a direct comparison between the physicochemical composition of consumer and its producer. An example of such relationship was found in the (...) order Hemiptera. No symbiosis exists when the consumer and producer belong to the same physicochemical type. On the other hand, if the types differ, extra- or intracellular symbiosis are usually found to exist. The conclusion is drawn that endosysmbiosis provides means for the compensation of this difference. (shrink)

If there is a single discipline of science calling the basic concepts of biology into question, it is without doubt microbiology. Indeed, developments in microbiology have recently forced us to rethink such fundamental concepts as the organism, individual, and genome. In this paper I show how microorganisms are changing our understanding of natural aggregations and develop the concept of a Darwinian population to embrace these discoveries. I start by showing that it is hard to set the boundaries of a Darwinian (...) population, and I suggest thinking of a Darwinian population as a relative property of a Darwinian individual. Then I argue, in contrast to the commonly held view, that Darwinian populations are multispecies units, and that in order to accept the multispecies account of Darwinian populations we have to separate fitness from natural selection. Finally, I show how all these ideas provide a theoretical framework leading to a more precise understanding of the ecology of endosymbiosis than is afforded by poetic metaphors such as ‘slavery’. (shrink)

This paper reviews and extends ideas of eukaryotization by endosymbiosis. These ideas are put within an historical context of processes that may have led up to eukaryotization and those that seem to have resulted from this process. Our starting point for considering the emergence and development of life as an organized system of chemical reactions should in the first place be in accordance with thermodynamic principles and hence should, as far as possible, be derived from these principles. One trend (...) to be observed is the ever-increasing complexity resulting in several layers of compartmentalization of the reaction system, either spatial (of which the eukaryotic cell is an example), or functional (as in the gradually deepening distinction between metabolic, enzymatic and information-storing functions within the cell). One of the causes of this complexification of living systems will have been the changes in environmental conditions, particularly the geochemical impoverishment of the biosphere during geological history, partly brought about by living systems themselves, and partly by the trend towards increasing efficiency and specificity of the reactions that occur. (shrink)

This paper aims to offer a new argument in defence bacterial species pluralism. To do so, I shall first present the particular issues derived from the conflict between the non-theoretical understanding of species as units of classification and the theoretical comprehension of them as units of evolution. Secondly, I shall justify the necessity of the concept of species for the bacterial world, and show how medicine and endosymbiotic evolutionary theory make use of different concepts of bacterial species due to their (...) distinctive purposes. Finally, I shall show how my argument provides a new source of defence for bacterial pluralism. (shrink)

Protistology, and evolutionary protistology in particular, is experiencing a golden research era. It is an extended one that can be dated back to the 1970s, which is when the molecular rebirth of microbial phylogeny began in earnest. John Archibald, a professor of evolutionary microbiology at Dalhousie University, focuses on the beautiful story of endosymbiosis in his book, John Archibald, One Plus One Equals One: Symbiosis and the Origin of Complex Life. However, this historical narrative could be treated as synecdochal (...) of how the molecular revolution has changed evolutionary biology forever, and that is how Archibald has structured his book. I will address the encompassing theme of molecular methods in detail, but also pay careful attention to the endosymbiosis thread in its own right. (shrink)

Both physiological and evolutionary criteria of biological individuality are underpinned by the idea that an individual is a functionally integrated whole. However, a precise account of functional integration has not been provided so far, and current notions are not developed in the details, especially in the case of composite systems. To address this issue, this paper focuses on the organisational dimension of two representative associations of prokaryotes: biofilms and the endosymbiosis between prokaryotes. Some critical voices have been raised against (...) the thesis that biofilms are biological individuals. Nevertheless, it has not been investigated which structural and functional obstacles may prevent them from being fully integrated physiological or evolutionary units. By contrast, the endosymbiotic association of different species of prokaryotes has the potential for achieving a different type of physiological integration based on a common boundary and interlocked functions. This type of association had made it possible, under specific conditions, to evolve endosymbionts into fully integrated organelles. This paper therefore has three aims: first, to analyse the organisational conditions and the physiological mechanisms that enable integration in prokaryotic associations; second, to discuss the organisational differences between biofilms and prokaryotic endosymbiosis and the types of integration they achieve; finally, to provide a more precise account of functional integration based on these case studies. (shrink)

We hypothesize that as one of the most consequential events in evolution, primary endosymbiosis accelerates lineage divergence, a process we refer to as the endosymbiotic ratchet. Our proposal is supported by recent work on the photosynthetic amoeba, Paulinella, that underwent primary plastid endosymbiosis about 124 Mya. This amoeba model allows us to explore the early impacts of photosynthetic organelle (plastid) origin on the host lineage. The current data point to a central role for effective population size (Ne) in (...) accelerating divergence post‐endosymbiosis due to limits to dispersal and reproductive isolation that reduce Ne, leading to local adaptation. We posit that isolated populations exploit different strategies and behaviors and assort themselves in non‐overlapping niches to minimize competition during the early, rapid evolutionary phase of organelle integration. The endosymbiotic ratchet provides a general framework for interpreting post‐endosymbiosis lineage evolution that is driven by disruptive selection and demographic and population shifts. Also see the video abstract here: https://youtu.be/gYXrFM6Zz6Q. (shrink)

Metagenomics bears upon all aspects of microbiology, including our understanding of mitochondrial and eukaryote origin. Recently, ribosomal protein phylogenies show the eukaryote host lineage – the archaeal lineage that acquired the mitochondrion – to branch within the archaea. Metagenomic studies are now uncovering new archaeal lineages that branch more closely to the host than any cultivated archaea do. But how do they grow? Carbon and energy metabolism as pieced together from metagenome assemblies of these new archaeal lineages, such as the (...) Deep Sea Archaeal Group (including Lokiarchaeota) and Bathyarchaeota, do not match the physiology of any cultivated microbes. Understanding how these new lineages live in their environment is important, and might hold clues about how mitochondria arose and how the eukaryotic lineage got started. Here we look at these exciting new metagenomic studies, what they say about archaeal physiology in modern environments, how they impact views on host‐mitochondrion physiological interactions at eukaryote origin. (shrink)

The significance of horizontal gene transfer (HGT) in eukaryotic evolution remains controversial. Although many eukaryotic genes are of bacterial origin, they are often interpreted as being derived from mitochondria or plastids. Because of their fixed gene pool and gene loss, however, mitochondria and plastids alone cannot adequately explain the presence of all, or even the majority, of bacterial genes in eukaryotes. Available data indicate that no insurmountable barrier to HGT exists, even in complex multicellular eukaryotes. In addition, the discovery of (...) both recent and ancient HGT events in all major eukaryotic groups suggests that HGT has been a regular occurrence throughout the history of eukaryotic evolution. A model of HGT is proposed that suggests both unicellular and early developmental stages as likely entry points for foreign genes into multicellular eukaryotes. (shrink)

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 induced by symbiosis, symbiogenesis, lateral gene transfer, hybridization or divergence with gene flow, and infective heredity, 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. The case studies presented examine topics including the origin of the eukaryotic cell and its organelles through symbiogenesis; the origin of algae through primary and secondary symbiosis and dinoflagellates through tertiary symbiosis; the superorganism and holobiont as units of evolution; how endosymbiosis induces speciation in multicellular life forms; transferrable and non-transferrable plasmids and how they symbiotically interact with their host; the means by which pro- and eukaryotic organisms transfer genes laterally (bacterial transformation, transduction and conjugation as well as transposons and other mobile genetic elements); hybridization and divergence with gene flow in sexually-reproducing individuals; current (human) microbiome and viriome studies that impact our knowledge concerning the evolution of organismal health and acquired immunity; and how symbiosis and symbiogenesis can be modelled in computational evolution. (shrink)

The realization that prokaryotes naturally and frequently disperse genes across steep taxonomic boundaries via lateral gene transfer gave wings to the idea that eukaryotes might do the same. Eukaryotes do acquire genes from mitochondria and plastids and they do transfer genes during the process of secondary endosymbiosis, the spread of plastids via eukaryotic algal endosymbionts. From those observations it, however, does not follow that eukaryotes transfer genes either in the same ways as prokaryotes do, or to a quantitatively similar (...) degree. An important illustration of the difference is that eukaryotes do not exhibit pangenomes, though prokaryotes do. Eukaryotes reveal no detectable cumulative effects of LGT, though prokaryotes do. A critical analysis suggests that something is deeply amiss with eukaryote LGT theories. In prokaryotes, genes from the environment can enter the genome via lateral gene transfer. In eukaryote genetics, natural variation comes from within the genome, not from the environment. Yet many reports claim that eukaryotes undergo LGT just like prokaryotes. Such claims do not withstand scrutiny and are probably untrue. (shrink)

In this article, I present two conceptual problems for Craver's mutual manipulability account of constitutive relevance in mechanisms. First, constitutive relevance threatens to imply causal relevance despite Craver (and Bechtel)'s claim that they are strictly distinct. Second, if (as is intuitively appealing) parthood is defined in terms of spatio-temporal inclusion, then the mutual manipulability account is prone to counterexamples, as I show by a case of endosymbiosis. I also present a methodological problem (a case of experimental underdetermination) and formulate (...) two partial, but fallible solutions based on the notions of parthood and synchronicity. (shrink)

Integrative mobile genetic elements (MGEs), such as transposons and insertion sequences, propagate within bacterial genomes, but persistence times in individual lineages are short. For long‐term survival, MGEs must continuously invade new hosts by horizontal transfer. Theoretically, MGEs that persist for millions of years in single lineages, and are thus subject to vertical inheritance, should not exist. Here we draw attention to an exception – a class of MGE termed REPIN. REPINs are non‐autonomous MGEs whose duplication depends on non‐jumping RAYT transposases. (...) Comparisons of REPINs and typical MGEs show that replication rates of REPINs are orders of magnitude lower, REPIN population size fluctuations correlate with changes in available genome space, REPIN conservation depends on RAYT function, and REPIN diversity accumulates within host lineages. These data lead to the hypothesis that REPINs form enduring, beneficial associations with eubacterial chromosomes. Given replicative nesting, our hypothesis predicts conflicts arising from the diverging effects of selection acting simultaneously on REPINs and host genomes. Evidence in support comes from patterns of REPIN abundance and diversity in two distantly related bacterial species. Together this bolsters the conclusion that REPINs are the genetic counterpart of mutualistic endosymbiotic bacteria. (shrink)

I hypothesize that the appearance of sex facilitated the merging of the endosymbiont and host genomes during early eukaryote evolution. Eukaryotes were formed by symbiosis between a bacterium that entered an archaeon, eventually giving rise to mitochondria. This entry was followed by the gradual transfer of most bacterial endosymbiont genes into the archaeal host genome. I argue that the merging of the mitochondrial genes into the host genome was vital for the evolution of genuine eukaryotes. At the time this process (...) commenced it was unprecedented and required a novel mechanism. I suggest that this mechanism was meiotic sex, and that its appearance might have been THE crucial step that enabled the evolution of proper eukaryotes from early endosymbiont containing proto‐eukaryotes. Sex might continue to be essential today for keeping genome insertions in check. Also see the video abstract here: https://youtu.be/aVMvWMpomac. (shrink)

Darwinian evolution can be simply stated: natural selection of inherited variations increasing differential reproduction. However, formulated thus, links with biochemistry, cell biology, ecology, and population dynamics remain unclear. To understand interactive contributions of chance and selection, higher levels of biological organization (e.g., endosymbiosis), complexities of competing selection forces, and emerging biological novelties (such as eukaryotes or meiotic sex), we must analyze actual examples. Focusing on mitochondria, I will illuminate how biology makes sense of life's evolution, and the concepts involved. (...) First, looking at the bacterium – mitochondrion transition: merging with an archaeon, it lost its independence, but played a decisive role in eukaryogenesis, as an extremely efficient aerobic ATP generator and internal ROS source. Second, surveying later mitochondrion adaptations and diversifications illustrates concepts such as constructive neutral evolution, dynamic interactions between endosymbionts and hosts, the contingency of life histories, and metabolic reprogramming. Without oxygen, mitochondria disappear; with (intermittent) oxygen diversification occurs in highly complex ways, especially upon (temporary) phototrophic substrate supply. These expositions show the Darwinian model to be a highly fruitful paradigm. (shrink)

Robustness is a fundamental property of biological systems, observed ubiquitously across species and at different levels of organization from gene regulation to ecosystem. The theory of biological robustness argues that robustness fosters evolv-ability and that together they entail various tradeoffs as well as characteristic architectures and mechanisms. We argue that classes of biological systems have evolved to enhance their robustness by extending their system boundary through a series of symbioses with foreign biological entities . A series of major biological innovations (...) has been achieved by events consistent with this framework: horizontal gene transfer, serial endosymbiosis, oocytes-mediated vertical infection, and host-symbiont mutualism for bacterial flora. Self-extending symbiosis contributes to robustness because symbiotic foreign biological entities can enhance the adaptative capacity of the system against environmental perturbations as well as contribute novel functions. In addition, evolutionary history indicates that the degree of symbiosis achieved has substantially changed from tight integration into the genome to loose integration as bacterial flora . The most dramatic example can be seen in the symbiosis of host immune system and bacterial flora in which substantial function of host defense depends on the proper maintenance of bacterial flora and its adaptive capability. Biological systems following this type of evolutionary path might have attained high levels of functionality, robustness, and evolvability. Thus, robustness, evolution, and self-extending symbiosis may form essential system principles for biology. (shrink)

The philosopher Graham Harman argues that contemporary debates about the nature of reality as such, and about the nature of objects in particular, can be meaningfully applied to social theory and practice. With Immaterialism, he has recently provided a case-based demonstration of how this could happen. But social theorists have compelling reasons to oppose object-oriented social theory’s 15 principles. Fidelity to Harman’s aesthetic foundationalism, and his particular use of serial endosymbiosis theory as a mechanism of social change, constrain the (...) very practices which it is supposed to enable. However, social theory stands to benefit from object-oriented philosophy through what we call posthuman relationism – characterised as a commitment to the reality of the nonhuman, but not divorced from the human. The emphasis in object-oriented social theory on how objects withdraw from cognitive or affective capture and representation needs to be tempered by an equal focus on how objects appeal. (shrink)

Selectionist evolutionary theory has often been faulted for not making novel predictions that are surprising, risky, and correct. I argue that it in fact exhibits the theoretical virtue of predictive capacity in addition to two other virtues: explanatory unification and model fitting. Two case studies show the predictive capacity of selectionist evolutionary theory: parallel evolutionary change in E. coli, and the origin of eukaryotic cells through endosymbiosis.

The consideration of ‘mutual benefits’ and partner cooperation have long been the accepted standpoint from which to draw inference about the onset, maintenance and breakdown of the coral‐algae endosymbiosis. In this paper, I review recent research into the climate‐induced breakdown of this important symbiosis (namely ‘coral bleaching’) that challenges the validity of this long‐standing belief. Indeed, I introduce a more parsimonious explanation, in which the coral host exerts a ‘controlled parasitism’ over its algal symbionts that is akin to an (...) enforced domestication arrangement. Far from being pathogenic, a range of well‐established cellular processes are reviewed that support the role of the coral host as an active ‘farmer’ of the energy‐rich photoassimilates from its captive symbionts. Importantly, this new paradigm reposes the deleterious bleaching response in terms of an envelope of environmental conditions in which the exploitative and captive measures of the coral host are severely restricted. The ramification of this new paradigm for developing management strategies that may assist the evolution of bleaching resistance in corals is discussed. (shrink)

This volume is the latest in a series of books and articles stretching back more than three decades on a theme quite startling in its claims and implications: that terrestrial life did not originate on Earth but arrived in the form of cells or bacteria from outer space. The idea of “panspermia,” that the seeds of life are spread from planet to planet, dates to the 19th century with the ideas of Lord Kelvin. It was championed by the Swedish physicist, (...) chemist, and Nobelist Svante Arrhenius at the beginning of the 20th century. Once scientists recognized the difficulties of life surviving in the conditions of interplanetary and interstellar space, by the 1960s a neo-panspermia became popular: not life itself, but prebiotic chemicals were the new seeds of life, made more likely by the discovery of numerous complex organic molecules in meteorites, comets, and interstellar molecular clouds. But the difficulties of synthesizing anything more complicated than amino acids in the wake of the famous Miller-Urey experiment in 1953 kept alive the idea that life itself may be spread throughout the universe. At the center of this work is Chandra Wickramasinghe, a research student of the maverick astronomer Fred Hoyle. In 1962 Hoyle became interested in the origin and nature of interstellar dust, in particular as found in dense molecular clouds, and he and Wickramasinghe set to work on the problem. They became convinced that dust could not form inside molecular clouds, but must have originated in the atmospheres of cool stars, protoplanetary discs, or supernova ejecta, a theory now widely accepted. It was the next steps that became increasingly controversial: that the spectroscopic signature of dust was best explained by complex biomolecules such as cellulose; that biomolecules were assembled into still more complex forms inside comets; and that the living cells and bacteria generated there were responsible for the origin of life on Earth. And not only that: Hoyle and Wickramasinghe argued that the delivery of bacteria from space continues, affecting both the origin and the ongoing evolution of life, and may even be responsible for certain diseases on Earth. These theories were not only reported in reputable scientific journals such as Nature, but also in popular books including Lifecloud (1978), Diseases from Space (1979), and Evolution from Space (1981). Biologists were not impressed; Lynn Margulis, not known for the timidity of her own theories such as endosymbiosis, called the first book “wanton, amusing, promiscuous fiction.”. (shrink)

Euglenids comprise a group of single‐celled eukaryotes with diverse modes of nutrition, including phagotrophy and photosynthesis. The level of morphological diversity present in this group provides an excellent system for demonstrating evolutionary transformations in morphological characters. This diversity also provides compelling evidence for major events in eukaryote evolution, such as the punctuated effects of secondary endosymbiosis and mutations in underlying developmental mechanisms. In this essay, we synthesize evidence for the origin, adaptive significance and diversification of the euglenid cytoskeleton, especially (...) pellicle ultrastructure, pellicle surface patterns, pellicle strip number and the feeding apparatus. We also highlight holes in our knowledge that must be filled before we are able to confidently describe euglenid cell biology and infer the earliest stages in euglenid evolution. Nonetheless, by possessing combinations of characters resulting from adaptive change and morphostasis, euglenids have retained key pieces of evidence necessary for reconstructing the early evolution and diversification of eukaryotic life. BioEssays 29:987–1000, 2007. © 2007 Wiley Periodicals, Inc. (shrink)

The initial relationships between organisms leading to endosymbiosis and the first eukaryote are currently a topic of hot debate. Here, I present a theory that offers a gradual scenario in which the origins of phagocytosis and mitochondria are intertwined in such a way that the evolution of one would not be possible without the other. In this scenario, the premitochondrial bacterial symbiont became initially associated with a protophagocytic host on the basis of cooperation to kill prey with symbiont‐produced toxins (...) and reactive oxygen species (ROS). Subsequently, the cooperation was focused on the digestion stage, through the acidification of the protophagocytic cavities via exportation of protons produced by the aerobic respiration of the symbiont. The host gained an improved phagocytic capacity and the symbiont received organic compounds from prey. As the host gradually lost its membrane energetics to develop lysosomal digestion, respiration was centralized in the premitochondrial symbiont for energy production for the consortium. (shrink)

Eukaryotic origins are inextricably linked with the arrival of a pre‐mitochondrion of alphaproteobacterial‐like ancestry. However, the nature of the “host” cell and the mode of entry are subject to heavy debate. It is becoming clear that the mutual adaptation of a relatively simple, archaeal host and the endosymbiont has been the defining influence at the beginning of the eukaryotic lineage; however, many still resist such symbiogenic models. In part 1, it is posited that a symbiotic stage before uptake (“pre‐symbiosis”) seems (...) essential to allow further metabolic integration of the two partners ending in endosymbiosis. Thus, the author argued against phagocytic mechanisms (in which the bacterium is prey or parasite) as the mode of entry. Such positions are still broadly unpopular. Here it is explained why. Evolutionary thinking, especially in the case of eukaryogenesis, is still dominated by anachronistic reasoning, in which highly derived protozoan organisms are seen as in some way representative of intermediate steps during eukaryotic evolution, hence poisoning the debate. This reasoning reflects a mind‐set that ignores that Darwinian evolution is a fundamentally historic process. Numerous examples of this kind of erroneous reasoning are given, and some basic precautions against its use are formulated. Also see the video abstract here https://youtu.be/ekqtNleVJpU. (shrink)

The origin of the eukaryotic cell nucleus and the selective forces that drove its evolution remain unknown and are a matter of controversy. Autogenous models state that both the nucleus and endoplasmic reticulum (ER) derived from the invagination of the plasma membrane, but most of them do not advance clear selective forces for this process. Alternative models proposing an endosymbiotic origin of the nucleus fail to provide a pathway fully compatible with our knowledge of cell biology. We propose here an (...) evolutionary scenario that reconciles both an ancestral endosymbiotic origin of the eukaryotic nucleus (endosymbiosis of a methanogenic archaeon within a fermentative myxobacterium) with an autogenous generation of the contemporary nuclear membrane and ER from the bacterial membrane. We specifically state two selective forces that operated sequentially during its evolution: (1) metabolic compartmentation to avoid deleterious co‐existence of anabolic (autotrophic synthesis by the methanogen) and catabolic (fermentation by the myxobacterium) pathways in the cell, and (2) avoidance of aberrant protein synthesis due to intron spreading in the ancient archaeal genome following mitochondrial acquisition and loss of methanogenesis. BioEssays 28: 525–533, 2006. © 2006 Wiley Periodicals, Inc. (shrink)

The philosopher Graham Harman argues that contemporary debates about the nature of reality as such, and about the nature of objects in particular, can be meaningfully applied to social theory and practice. With Immaterialism, he has recently provided a case-based demonstration of how this could happen. But social theorists have compelling reasons to oppose object-oriented social theory’s 15 principles. Fidelity to Harman’s aesthetic foundationalism, and his particular use of serial endosymbiosis theory as a mechanism of social change, constrain the (...) very practices which it is supposed to enable. However, social theory stands to benefit from object-oriented philosophy through what we call posthuman relationism – characterised as a commitment to the reality of the nonhuman, but not divorced from the human. The emphasis in object-oriented social theory on how objects withdraw from cognitive or affective capture and representation needs to be tempered by an equal focus on how objects appeal. (shrink)

Eukaryogenesis is widely viewed as an improbable evolutionary transition uniquely affecting the evolution of life on this planet. However, scientific and popular rhetoric extolling this event as a singularity lacks rigorous evidential and statistical support. Here, we question several of the usual claims about the specialness of eukaryogenesis, focusing on both eukaryogenesis as a process and its outcome, the eukaryotic cell. We argue in favor of four ideas. First, the criteria by which we judge eukaryogenesis to have required a genuinely (...) unlikely series of events 2 billion years in the making are being eroded by discoveries that fill in the gaps of the prokaryote:eukaryote “discontinuity.” Second, eukaryogenesis confronts evolutionary theory in ways not different from other evolutionary transitions in individuality; parallel systems can be found at several hierarchical levels. Third, identifying which of several complex cellular features confer on eukaryotes a putative richer evolutionary potential remains an area of speculation: various keys to success have been proposed and rejected over the five-decade history of research in this area. Fourth, and perhaps most importantly, it is difficult and may be impossible to eliminate eukaryocentric bias from the measures by which eukaryotes as a whole are judged to have achieved greater success than prokaryotes as a whole. Overall, we question whether premises of existing theories about the uniqueness of eukaryogenesis and the greater evolutionary potential of eukaryotes have been objectively formulated and whether, despite widespread acceptance that eukaryogenesis was “special,” any such notion has more than rhetorical value. (shrink)

Numerous scenarios explain the origin of the eukaryote cell by fusion or endosymbiosis between an archaeon and a bacterium (and sometimes a third partner). We evaluate these hypotheses using the following three criteria. Can the data be explained by the null hypothesis that new features arise sequentially along a stem lineage? Second, hypotheses involving an archaeon and a bacterium should undergo standard phylogenetic tests of gene distribution. Third, accounting for past events by processes observed in modern cells is preferable (...) to postulating unknown processes that have never been observed. For example, there are many eukaryote examples of bacteria as endosymbionts or endoparasites, but none known in archaea. Strictly post‐hoc hypotheses that ignore this third criterion should be avoided. Applying these three criteria significantly narrows the number of plausible hypotheses. Given current knowledge, our conclusion is that the eukaryote lineage must have diverged from an ancestor of archaea well prior to the origin of the mitochondrion. Significantly, the absence of ancestrally amitochondriate eukaryotes (archezoa) among extant eukaryotes is neither evidence for an archaeal host for the ancestor of mitochondria, nor evidence against a eukaryotic host. BioEssays 29: 74–84, 2007. © 2006 Wiley Periodicals, Inc. (shrink)

Exaptations are adaptations that have undergone a major change in function. By recruiting genes from sources originally unrelated to vision, exaptation has allowed for sudden and critical photosensory innovations, such as lenses, photopigments, and photoreceptors. Here we review new or neglected findings, with an emphasis on unicellular eukaryotes (protists), to illustrate how exaptation has shaped photoreception across the tree of life. Protist phylogeny attests to multiple origins of photoreception, as well as the extreme creativity of evolution. By appropriating genes and (...) even entire organelles from foreign organisms via lateral gene transfer and endosymbiosis, protists have cobbled photoreceptors and eyespots from a diverse set of ingredients. While refinement through natural selection is paramount, exaptation helps illustrate how novelties arise in the first place, and is now shedding light on the origins of photoreception itself. -/- . (shrink)

Selectionist evolutionary theory has often been faulted for not making novel predictions that are surprising, risky, and correct. I argue that it in fact exhibits the theoretical virtue of predictive capacity in addition to two other virtues: explanatory unification and model fitting. Two case studies show the predictive capacity of selectionist evolutionary theory: parallel evolutionary change in E. coli, and the origin of eukaryotic cells through endosymbiosis.

Phylogenetic models traditionally represent the history of life as having a strictly-branching tree structure. However, it is becoming increasingly clear that the history of life is often not strictly-branching; lateral gene transfer, endosymbiosis, and hybridization, for example, can all produce lateral branching events. There is thus motivation to allow phylogenetic models to have a reticulate structure. One proposal involves the reconciliation of genealogical discordance. Briefly, this method uses patterns of disagreement – discordance – between trees of different genes to (...) add lateral branching events to phylogenetic trees of taxa, and to estimate the most likely cause of these events. I use this practice to argue for: (1) a need for expanded accounts of multiple-models idealization, (2) a distinction between automatic and manual de-idealization, and (3) recognition that idealization may serve the meso-level aims of science in a different way than hitherto acknowledged. (shrink)

Mitochondrial genomes represent relict bacterial genomes derived from a progenitor α‐proteobacterium that gave rise to all mitochondria through an ancient endosymbiosis. Evolution has massively reduced these genomes, yet despite relative simplicity their organization and expression has developed considerable novelty throughout eukaryotic evolution. Few organisms have reengineered their mitochondrial genomes as thoroughly as the protist lineage of dinoflagellates. Recent work reveals dinoflagellate mitochondrial genomes as likely the most gene‐impoverished of any free‐living eukaryote, encoding only two to three proteins. The organization (...) and expression of these genomes, however, is far from the simplicity their gene content would suggest. Gene duplication, fragmentation, and scrambling have resulted in an inflated and complex genome organization. Extensive RNA editing then recodes gene transcripts, and trans‐splicing is required to assemble full‐length transcripts for at least one fragmented gene. Even after these processes, messenger RNAs (mRNAs) lack canonical start codons and most transcripts have abandoned stop codons altogether. (shrink)

During evolution, the genomes of eukaryotic cells have undergone major restructuring to meet the new regulatory challenges associated with compartmentalization of the genetic material in the nucleus and the organelles acquired by endosymbiosis (mitochondria and plastids). Restructuring involved the loss of dispensable or redundant genes and the massive translocation of genes from the ancestral organelles to the nucleus. Genomics and bioinformatic data suggest that the process of DNA transfer from organelles to the nucleus still continues, providing raw material for (...) evolutionary tinkering in the nuclear genome. Recent reconstruction of these events in the laboratory has provided a unique tool to observe genome evolution in real time and to study the molecular mechanisms by which plastid genes are converted into functional nuclear genes. Here, we summarize current knowledge about plastid‐to‐nuclear gene transfer in the context of genome evolution and discuss new insights gained from experiments that recapitulate endosymbiotic gene transfer in the laboratory. BioEssays 30:556–566, 2008. © 2008 Wiley Periodicals, Inc. (shrink)

Proteins are targeted to plastids by N‐terminal transit peptides, which are recognized by protein import complexes in the organelle membranes. Historically, transit peptide properties have been defined from vascular plant sequences, but recent large‐scale genome sequencing from the many plastid‐containing lineages across the tree of life has provided a much broader representation of targeted proteins. This includes the three lineages containing primary plastids (plants and green algae, rhodophytes and glaucophytes) and also the seven major lineages that contain secondary plastids, “secondhand” (...) plastids derived through eukaryotic endosymbiosis. Despite this extensive spread of plastids throughout Eukaryota, an N‐terminal transit peptide has been maintained as an essential plastid‐targeting motif. This article provides the first global comparison of transit peptide composition and summarizes conservation of some features, the loss of an ancestral motif from the green lineages including plants, and modifications to transit peptides that have occurred in secondary and even tertiary plastids. BioEssays 29:1048–1058, 2007. © 2007 Wiley Periodicals, Inc. (shrink)

Diatoms are important protists that generate one fifth of the oxygen produced annually on earth. These aquatic organisms likely derived from a secondary endosymbiosis event, and they display peculiar genomic and structural features that reflect their chimeric origin. Diatoms were one of the first models of cell division and these early studies revealed a range of interesting features including a unique acentriolar microtubule‐organising centre. Unfortunately, almost nothing is known at the molecular level, in contrast to the advances in other (...) experimental organisms. Recently the full genome sequences of two diatoms have been annotated and molecular tools have been developed. These resources offer new possibilities to re‐investigate the mechanisms of cell division in diatoms by recruiting information from more intensively studied organisms. A renaissance of the topic is further justified by the current interest in diatoms as a source of biofuels and for understanding massive diatom proliferation events in response to environmental stimuli. (shrink)

Arbuscular mycorrhiza (AM), a type of plant‐fungal endosymbiosis, and nodulation, a bacterial‐plant endosymbiosis, are the most ubiquitous symbioses on earth. Recent findings have established part of a shared genetic basis underlying these interactions. Here, we approach root endosymbioses through the lens of the homology and modularity concepts aiming at further clarifying the proximate and ultimate causes for the establishment of these biological systems. We review the genetics that underlie interspecific signaling and its concomitant shift in genetic programs for (...) either partner. Also, through the comparative analysis of genetic modules shared by AM and nodulation symbioses, we identify fundamental nodes in these networks, suggesting the elemental steps that may have permitted symbiotic adaptation. Here, we show that this approach, allied to recent technical advances in the study of genetic systems architecture, can provide clear testable hypotheses for the advancement of our understanding on the evolution and development of symbiotic systems. (shrink)

We highlight the deep ecology movement, inspired on ecological knowledge but mainly on the life-style of the ecological and biological field-worker. Its creator, the Norwegian philosopher Arne Naess, stresses that human and no human beings have, at least, one kind of right in common: namely the ‘right’ to express its own nature, to live and blossom. This idea shows the inspiration from perseverare in suo esse, from Baruch Spinoza’s Ethics. But beyond this Spinozan influence, the striving for expression of one’s (...) own nature is interpreted from the perspective of present evolutionism and endosymbiosis. Even though, scientific knowledge, if necessary, is considered limited. Thus, this movement should be regarded as ecophilosophical rather than ecological, as a kind of sophia orwisdom. In turn, many supporters of conservation biology (following Michael Soulé) associate their science with ecosophy, not encouraging the dichotomy fact/value. Conservation biology axioms such as: evolution in valuable, organism’s diversity is good, premature extinction of species populations is negative, etc., have been inspired on the deep ecology movement. The consideration of the terms biodiversity, evolution or biosphere as thick ethical concepts (following Hillary Putnam), shows this integration of the descriptive and the normative. (shrink)

The placozoan Trichoplax adhaerens is a tiny hairy plate and more simply organized than any other living metazoan. After its original description by F.E. Schulze in 1883, it attracted attention as a potential model for the ancestral state of metazoan organization, the “Urmetazoon”. Trichoplax lacks any kind of symmetry, organs, nerve cells, muscle cells, basal lamina, and extracellular matrix. Furthermore, the placozoan genome is the smallest (not secondarily reduced) genome of all metazoan genomes. It harbors a remarkably rich diversity of (...) genes and has been considered the best living surrogate for a metazoan ancestor genome. The phylum Placozoa presently harbors three formally described species, while several dozen “cryptic” species are yet awaiting their description. The phylogenetic position of placozoans has recently become a contested arena for modern phylogenetic analyses and view‐driven claims. Trichoplax offers unique prospects for understanding the minimal requirements of metazoan animal organization and their corresponding malfunctions. (shrink)

The acoel worm Symsagittifera roscoffensis, an early offshoot of the Bilateria and the only well‐studied marine acoel that lives in a photosymbiotic relationship, exhibits a centralized nervous system, brain regeneration, and a wide repertoire of complex behaviors such as circatidal rhythmicity, photo/geotaxis, and social interactions. While this animal can be collected by the thousands and is studied historically, significant progress is made over the last decade to develop it as an emerging marine model. The authors here present the feasibility of (...) culturing it in the laboratory and describe the progress made on different areas, including genomic and tissue architectures, highlighting the associated challenges. In light of these developments, and on the ability to access abundant synchronized embryos, the authors put forward S. roscoffensis as a marine system to revisit questions in the areas of photosymbiosis, regeneration, chronobiology, and the study of complex behaviors from a molecular and evolutionary perspective. (shrink)

Both the concept of a Darwinian tree of life (TOL) and the possibility of its accurate reconstruction have been much criticized. Criticisms mostly revolve around the extensive occurrence of lateral gene transfer (LGT), instances of uptake of complete organisms to become organelles (with the associated subsequent gene transfer to the nucleus), as well as the implications of more subtle aspects of the biological species concept. Here we argue that none of these criticisms are sufficient to abandon the valuable TOL concept (...) and the biological realities it captures. Especially important is the need to conceptually distinguish between organismal trees and gene trees, which necessitates incorporating insights of widely occurring LGT into modern evolutionary theory. We demonstrate that all criticisms, while based on important new findings, do not invalidate the TOL. After considering the implications of these new insights, we find that the contours of evolution are best represented by a TOL. (shrink)

Prokaryotic genomes of endosymbionts and parasites are examples of naturally evolved minimal cells, the study of which can shed light on life in its minimum form. Their diverse biology, their lack of a large set of orthologous genes and the existence of essential linage (and environmentally) specific genes all illustrate the diversity of genes building up naturally evolved minimal cells. This conclusion is reinforced by the fact that sometimes the same essential function is performed by genes from different evolutionary origins. (...) Nevertheless, all cells perform a set of life‐essential functions however different their cell machinery and environment in which they thrive. An upcoming challenge for biologists will be to discern, by studying differences and similarities in current biodiversity, how cells with reduced genomes have adapted while retaining all basic life‐supporting functions. (shrink)

Some nuclear‐encoded proteins are imported into higher plant plastids via the endomembrane (EM) system. Compared with multi‐protein Toc and Tic translocons required for most plastid protein import, the relatively uncomplicated nature of EM trafficking led to suggestions that it was the original transport mechanism for nuclear‐encoded endosymbiont proteins, and critical for the early stages of plastid evolution. Its apparent simplicity disappears, however, when EM transport is considered in light of selective constraints likely encountered during the conversion of stable endosymbionts into (...) fully integrated organelles. From this perspective it is more parsimonious to presume the early evolution of post‐translational protein import via simpler, ancestral forms of modern Toc and Tic plastid translocons, with EM trafficking arising later to accommodate glycosylation and/or protein targeting to multiple cellular locations. This hypothesis is supported by both empirical and comparative data, and is consistent with the relative paucity of EM‐based transport to modern primary plastids. (shrink)

The new discipline of exobiology formed from the intertwining of origin of life research with the search for life or its building blocks on other planets, from 1957-1973. The field was inherently highly interdisciplinary, yet it coalesced very quickly and was responsible in its first twenty years for numerous important contributions to twentieth century life science and planetary sciences such as climatology, the study of mass extinctions, etc. NASA played a very important role in catalyzing the rapid consolidation of exobiology, (...) both through research grants and through sponsored meetings that overcame disciplinary boundaries, bringing together scientists from diverse backgrounds. The presence of a handful of prominent senior scientists such as Joshua Lederberg, Melvin Calvin and Norman Horowitz helped gain credibility for exobiology, in the face of criticism and competition from existing life sciences disciplines. Tensions within the exobiology research community and between NASA-funded science and the academic research community are explored, as are such milestones of discipline formation as journals and professional societies. (shrink)