Managing expectationsFluke: Chance, Chaos, and Why Everything We Do Matters Brian Klaas Scribner, 2024. 336 pp.

A political scientist urges readers to embrace the chaos and complexity of life.

The eco-evolutionary origins of life.

The origin of life remains one of the greatest enigmas in science. The immense leap in complexity between prebiotic soup and cellular life challenges historically "chemistry-forward" and "biology-backwards" approaches. Evolution must have bridged this gap in complexity, so understanding factors that influence evolutionary outcomes is critical for exploring life's emergence. Here, we review insights from ecology and evolution and their application throughout abiogenesis. In particular, we discuss how ecological and evolutionary constraints shape the evolution of biological innovation. We propose an "eco-evolutionary" approach, which is agnostic towards particular chemistries or environments and instead explores the several ways that an evolvable system may emerge and gain complexity.

The Cuatro Ciénegas Basin.

In the state of Coahuila, Mexico, there is a very special place, just 290 km from the border with Texas: the oasis in the Cuatro Ciénegas Basin. Souza et al. describe how the geology of the basin has given rise to a unique chemistry and a community of organisms that have survived for eons and are found nowhere else on Earth.

Multispecies interactions shape the transition to multicellularity.

The origin of multicellularity transformed the adaptive landscape on Earth, opening diverse avenues for further innovation. The transition to multicellular life is understood as the evolution of cooperative groups which form a new level of individuality. Despite the potential for community-level interactions, most studies have not addressed the competitive context of this transition, such as competition between species. Here, we explore how interspecific competition shapes the emergence of multicellularity in an experimental system with two yeast species, Saccharomyces cerevisiae and Kluyveromyces lactis, where multicellularity evolves in response to selection for faster settling ability. We find that the multispecies context slows the rate of the transition to multicellularity, and the transition to multicellularity significantly impacts community composition. Multicellular K. lactis emerges first and sweeps through populations in monocultures faster than in cocultures with S. cerevisiae. Following the transition, the between-species competitive dynamics shift, likely in part to intraspecific cooperation in K. lactis. Hence, we document an eco-evolutionary feedback across the transition to multicellularity, underscoring how ecological context is critical for understanding the causes and consequences of innovation. By including two species, we demonstrate that cooperation and competition across several biological scales shapes the origin and persistence of multicellularity.

Experimental evolution in the cyanobacterium Trichormus variabilis: increases in size and morphological diversity.

Cyanobacteria morphology has apparently remained almost unchanged for billions of years, exhibiting remarkable evolutionary stasis. Cyanobacteria appear to have reached their maximum morphological complexity in terms of size, modes of multicellularity, and cellular types by ~2 Ga. This contrasts with the increased complexity observed in other multicellular lineages, such as plants. Using experimental evolution, we show that morphological diversity can rapidly evolve in a species of filamentous cyanobacteria. Since size has such significance with regard to organismal complexity, we subjected the heterocyst-forming cyanobacterium Trichornus variabilis (syn. Anabaena variabilis) to selection for larger size. We observed increases in size of more than 30-fold, relative to the ancestral population, after 45 cycles of selection. Two distinguishable nascent morphological elaborations were identified in all the selected populations: Tangle (long, tangled filaments) and Cluster (clusters of short filaments) morphology. Growth from single cells indicates heritability of the evolved Tangle and Cluster morphological phenotypes. Cyanobacteria evolutionary conservatism is ascribed to developmental constraints, slow evolution rates, or ecological flexibility. These results open opportunities to study possibilities and constraints for the evolution of higher integrated biological levels of organization within this lineage.

Disentangling a metabolic cross-feeding in a halophilic archaea-bacteria consortium.

Microbial syntrophy, a cooperative metabolic interaction among prokaryotes, serves a critical role in shaping communities, due to the auxotrophic nature of many microorganisms. Syntrophy played a key role in the evolution of life, including the hypothesized origin of eukaryotes. In a recent exploration of the microbial mats within the exceptional and uniquely extreme Cuatro Cienegas Basin (CCB), a halophilic isolate, designated as AD140, emerged as a standout due to its distinct growth pattern. Subsequent genome sequencing revealed AD140 to be a co-culture of a halophilic archaeon from the Halorubrum genus and a marine halophilic bacterium, Marinococcus luteus, both occupying the same ecological niche. This intriguing coexistence hints at an early-stage symbiotic relationship that thrives on adaptability. By delving into their metabolic interdependence through genomic analysis, this study aims to uncover shared characteristics that enhance their symbiotic association, offering insights into the evolution of halophilic microorganisms and their remarkable adaptations to high-salinity environments.

Loss-of-heterozygosity facilitates a fitness valley crossing in experimentally evolved multicellular yeast.

Determining how adaptive possibilities do or do not become evolutionary realities is central to understanding the tempo and mode of evolutionary change. Some of the simplest evolutionary landscapes arise from underdominance at a single locus where the fitness valley consists of only one less-fit genotype. Despite their potential for rapid evolutionary change, few such examples have been investigated. We capitalized on an experimental system in which a significant evolutionary shift, the transition from uni-to-multicellularity, was observed in asexual diploid populations of Saccharomyces cerevisiae experimentally selected for increased settling rates. The multicellular phenotype results from recessive single-locus mutations that undergo loss-of-heterozygosity (LOH) events. By reconstructing the necessary heterozygous intermediate steps, we found that the evolution of multicellularity involves a decrease in size during the first steps. Heterozygous genotypes are 20% smaller in size than genotypes with functional alleles. Nevertheless, populations of heterozygotes give rise to multicellular genotypes more readily than unicellular genotypes with two functional alleles, by rapid LOH events. LOH drives adaptation that may enable rapid evolution in diploid yeast. Together these results show discordance between the phenotypic and genotypic multicellular transition. The evolutionary path to multicellularity, and the adaptive benefits of increased size, requires initial size reductions.

Adaptation and Exaptation: From Small Molecules to Feathers.

Evolution works by adaptation and exaptation. At an organismal level, exaptation and adaptation are seen in the formation of organelles and the advent of multicellularity. At the sub-organismal level, molecular systems such as proteins and RNAs readily undergo adaptation and exaptation. Here we suggest that the concepts of adaptation and exaptation are universal, synergistic, and recursive and apply to small molecules such as metabolites, cofactors, and the building blocks of extant polymers. For example, adenosine has been extensively adapted and exapted throughout biological evolution. Chemical variants of adenosine that are products of adaptation include 2' deoxyadenosine in DNA and a wide array of modified forms in mRNAs, tRNAs, rRNAs, and viral RNAs. Adenosine and its variants have been extensively exapted for various functions, including informational polymers (RNA, DNA), energy storage (ATP), metabolism (e.g., coenzyme A), and signaling (cyclic AMP). According to Gould, Vrba, and Darwin, exaptation imposes a general constraint on interpretation of history and origins; because of exaptation, extant function should not be used to explain evolutionary history. While this notion is accepted in evolutionary biology, it can also guide the study of the chemical origins of life. We propose that (i) evolutionary theory is broadly applicable from the dawn of life to the present time from molecules to organisms, (ii) exaptation and adaptation were important and simultaneous processes, and (iii) robust origin of life models can be constructed without conflating extant utility with historical basis of origins.

Plasmid hypermutation using a targeted artificial DNA replisome.

Extensive exploration of a protein's sequence space for improved or new molecular functions requires in vivo evolution with large populations. But disentangling the evolution of a target protein from the rest of the proteome is challenging. Here, we designed a protein complex of a targeted artificial DNA replisome (TADR) that operates in live cells to processively replicate one strand of a plasmid with errors. It enhanced mutation rates of the target plasmid up to 2.3 × 105-fold with only a 78-fold increase in off-target mutagenesis. It was used to evolve itself to increase error rate and increase the efficiency of an efflux pump while simultaneously expanding the substrate repertoire. TADR enables multiple simultaneous substitutions to discover functions inaccessible by accumulating single substitutions, affording potential for solving hard problems in molecular evolution and developing biologic drugs and industrial catalysts.

The landscape of innovation in bacteria, battleships, and beyond.

We draw lessons from microbial experimental evolution and naval warfare to improve the understanding of innovation in financial markets. Major financial innovations often arise without explicit societal planning because novel approaches can be favored by markets, in a manner strikingly parallel to natural selection. We utilize the concept of an adaptive landscape to characterize environments that increase the speed and magnitude of innovation. We apply this adaptive landscape framework to innovation in portfolio management. We create a general taxonomy for understanding and nurturing innovation.

Lessons from movement ecology for the return to work: Modeling contacts and the spread of COVID-19.

Human behavior (movement, social contacts) plays a central role in the spread of pathogens like SARS-CoV-2. The rapid spread of SARS-CoV-2 was driven by global human movement, and initial lockdown measures aimed to localize movement and contact in order to slow spread. Thus, movement and contact patterns need to be explicitly considered when making reopening decisions, especially regarding return to work. Here, as a case study, we consider the initial stages of resuming research at a large research university, using approaches from movement ecology and contact network epidemiology. First, we develop a dynamical pathogen model describing movement between home and work; we show that limiting social contact, via reduced people or reduced time in the workplace are fairly equivalent strategies to slow pathogen spread. Second, we develop a model based on spatial contact patterns within a specific office and lab building on campus; we show that restricting on-campus activities to labs (rather than labs and offices) could dramatically alter (modularize) contact network structure and thus, potentially reduce pathogen spread by providing a workplace mechanism to reduce contact. Here we argue that explicitly accounting for human movement and contact behavior in the workplace can provide additional strategies to slow pathogen spread that can be used in conjunction with ongoing public health efforts.

Archaeal Communities: The Microbial Phylogenomic Frontier.

Archaea are a unique system for investigating the diversity of life. There are the most diverse group of organisms with the longest evolutionary history of life on Earth. Phylogenomic investigations reveal the complex evolutionary history of Archaea, overturning longstanding views of the history of life. They exist in the harshest environments and benign conditions, providing a system to investigate the basis for living in extreme environments. They are frequently members of microbial communities, albeit generally rare. Archaea were central in the evolution of Eukaryotes and can be used as a proxy for studying life on other planets. Future advances will depend not only upon phylogenomic studies but also on a better understanding of isolation and cultivation techniques.

Evolutionary innovation using EDGE, a system for localized elevated mutagenesis.

Mutations arising across the whole genome can hinder the emergence of evolutionary innovation required for adaptation because many mutations are deleterious. This trade-off is overcome by elevated mutagenesis to localized loci. Examples include phase variation and diversity-generating retroelements. However, these mechanisms are rare in nature; and all have narrow mutational spectra limiting evolutionary innovation. Here, we engineer a platform of Experimental Designed Genic Evolution (EDGE) to study the potential for evolutionary novelty at a single locus. Experimental evolution with EDGE shows that bacterial resistance to a novel antibiotic readily evolves, provided that elevated mutagenesis is focused on a relevant gene. A model is proposed to account for the cost and benefit of such single loci to adaptation in a changing environment and explains their high mutation rates, limited innovation, and the rarity of localized mutagenesis in nature. Overall, our results suggest that localized mutation systems can facilitate continuing adaptive evolution without necessarily restricting the spectrum of mutations. EDGE has utility in dissecting the complex process of adaptation with its localized, efficient evolution.

Plastic multicellular development of Myxococcus xanthus: genotype-environment interactions in a physical gradient.

In order to investigate the contribution of the physical environment to variation in multicellular development of Myxococcus xanthus, phenotypes developed by different genotypes in a gradient of substrate stiffness conditions were quantitatively characterized. Statistical analysis showed that plastic phenotypes result from the genotype, the substrate conditions and the interaction between them. Also, phenotypes were expressed in two distinguishable scales, the individual and the population levels, and the interaction with the environment showed scale and trait specificity. Overall, our results highlight the constructive role of the physical context in the development of microbial multicellularity, with both ecological and evolutionary implications.

Symbiont evolution during the free-living phase can improve host colonization.

For micro-organisms cycling between free-living and host-associated stages, where reproduction occurs in both of these lifestyles, an interesting inquiry is whether evolution during the free-living stage can be positively pleiotropic to microbial fitness in a host environment. To address this topic, the squid host Euprymna tasmanica and the marine bioluminescent bacterium Vibrio fischeri were utilized. Microbial ecological diversification in static liquid microcosms was used to simulate symbiont evolution during the free-living stage. Thirteen genetically distinct V. fischeri strains from a broad diversity of ecological sources (e.g. squid light organs, fish light organs and seawater) were examined to see if the results were reproducible in many different genetic settings. Genetic backgrounds that are closely related can be predisposed to considerable differences in how they respond to similar selection pressures. For all strains examined, new mutations with striking and facilitating effects on host colonization arose quickly during microbial evolution in the free-living stage, regardless of the ecological context under consideration for a strain's genetic background. Microbial evolution outside a host environment promoted host range expansion, improved host colonization for a micro-organism, and diminished the negative correlation between biofilm formation and motility.

Adaptation, chance, and history in experimental evolution reversals to unicellularity.

Evolution is often deemed irreversible. The evolution of complex traits that require many mutations makes their reversal unlikely. Even in simpler traits, reversals might become less likely as neutral or beneficial mutations, with deleterious effects in the ancestral context, become fixed in the novel background. This is especially true in changes that involve large reorganizations of the organism and its interactions with the environment. The evolution of multicellularity involves the reorganization of previously autonomous cells into a more complex organism; despite the complexity of this change, single cells have repeatedly evolved from multicellular ancestors. These repeated reversals to unicellularity undermine the generality of Dollo's law. In this article, we evaluated the dynamics of reversals to unicellularity from recently evolved multicellular phenotypes of the brewers yeast Saccharomyces cerevisae. Even though multicellularity in this system evolved recently, it involves the evolution of new levels of selection. Strong selective pressures against multicellularity lead to rapid reversibility to single cells in all of our replicate lines, whereas counterselection favoring multicellularity led to minimal reductions to the rates of reversal. History and chance played an important role in the tempo and mode of reversibility, highlighting the interplay of deterministic and stochastic events in evolutionary reversals.

The lost world of Cuatro Ciénegas Basin, a relictual bacterial niche in a desert oasis.

Barriers to microbial migrations can lead adaptive radiations and increased endemism. We propose that extreme unbalanced nutrient stoichiometry of essential nutrients can be a barrier to microbial immigration over geological timescales. At the oasis in the Cuatro Ciénegas Basin in Mexico, nutrient stoichiometric proportions are skewed given the low phosphorus availability in the ecosystem. We show that this endangered oasis can be a model for a lost world. The ancient niche of extreme unbalanced nutrient stoichiometry favoured survival of ancestral microorganisms. This extreme nutrient imbalance persisted due to environmental stability and low extinction rates, generating a diverse and unique bacterial community. Several endemic clades of Bacillus invaded the Cuatro Cienegas region in two geological times, the late Precambrian and the Jurassic. Other lineages of Bacillus, Clostridium and Bacteroidetes migrated into the basin in isolated events. Cuatro Ciénegas Basin conservation is vital to the understanding of early evolutionary and ecological processes.

The Cost of Being Big: Local Competition, Importance of Dispersal, and Experimental Evolution of Reversal to Unicellularity.

Multicellularity provides multiple benefits. Nonetheless, unicellularity is ubiquitous, and there have been multiple cases of evolutionary reversal to a unicellular organization. In this article, we explore some of the costs of multicellularity as well as the possibility and dynamics of evolutionary reversals to unicellularity. We hypothesize that recently evolved multicellular organisms would face a high cost of increased competition for local resources in spatially structured environments because of larger size and increased cell densities. To test this hypothesis we conducted competition assays, computer simulations, and selection experiments using isolates of Saccharomyces cerevisiae that recently evolved multicellularity. In well-mixed environments, multicellular isolates had lower growth rates relative to their unicellular ancestor because of limitations of space and resource acquisition. In structured environments with localized resources, cells in both multicellular and unicellular isolates grew at a similar rate. Despite similar growth, higher local density of cells in multicellular groups led to increased competition and higher fitness costs in spatially structured environments. In structured environments all of the multicellular isolates rapidly evolved a predominantly unicellular life cycle, while in well-mixed environments reversal was more gradual. Taken together, these results suggest that a lack of dispersal, leading to higher local competition, might have been one of the main constraints in the evolution of early multicellular forms.

Exploring the evolution of multicellularity in Saccharomyces cerevisiae under bacteria environment: An experimental phylogenetics approach.

There have been over 25 independent unicellular to multicellular evolutionary transitions, which have been transformational in the complexity of life. All of these transitions likely occurred in communities numerically dominated by unicellular organisms, mostly bacteria. Hence, it is reasonable to expect that bacteria were involved in generating the ecological conditions that promoted the stability and proliferation of the first multicellular forms as protective units. In this study, we addressed this problem by analyzing the occurrence of multicellularity in an experimental phylogeny of yeasts (Sacharomyces cerevisiae) a model organism that is unicellular but can generate multicellular clusters under some conditions. We exposed a single ancestral population to periodic divergences, coevolving with a cocktail of environmental bacteria that were inoculated to the environment of the ancestor, and compared to a control (no bacteria). We quantified culturable microorganisms to the level of genera, finding up to 20 taxa (all bacteria) that competed with the yeasts during diversification. After 600 generations of coevolution, the yeasts produced two types of multicellular clusters: clonal and aggregative. Whereas clonal clusters were present in both treatments, aggregative clusters were only present under the bacteria treatment and showed significant phylogenetic signal. However, clonal clusters showed different properties if bacteria were present as follows: They were more abundant and significantly smaller than in the control. These results indicate that bacteria are important modulators of the occurrence of multicellularity, providing support to the idea that they generated the ecological conditions-promoting multicellularity.

The Evolution of Molecular Compatibility between Bacteriophage ΦX174 and its Host.

Viruses rely upon their hosts for biosynthesis of viral RNA, DNA and protein. This dependency frequently engenders strong selection for virus genome compatibility with potential hosts, appropriate gene regulation and expression necessary for a successful infection. While bioinformatic studies have shown strong correlations between codon usage in viral and host genomes, the selective factors by which this compatibility evolves remain a matter of conjecture. Engineered to include codons with a lesser usage and/or tRNA abundance within the host, three different attenuated strains of the bacterial virus ФX174 were created and propagated via serial transfers. Molecular sequence data indicate that biosynthetic compatibility was recovered rapidly. Extensive computational simulations were performed to assess the role of mutational biases as well as selection for translational efficiency in the engineered phage. Using bacteriophage as a model system, we can begin to unravel the evolutionary processes shaping codon compatibility between viruses and their host.