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.

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.

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.

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.

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.

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.

Geometry shapes evolution of early multicellularity.

Organisms have increased in complexity through a series of major evolutionary transitions, in which formerly autonomous entities become parts of a novel higher-level entity. One intriguing feature of the higher-level entity after some major transitions is a division of reproductive labor among its lower-level units in which reproduction is the sole responsibility of a subset of units. Although it can have clear benefits once established, it is unknown how such reproductive division of labor originates. We consider a recent evolution experiment on the yeast Saccharomyces cerevisiae as a unique platform to address the issue of reproductive differentiation during an evolutionary transition in individuality. In the experiment, independent yeast lineages evolved a multicellular "snowflake-like" cluster formed in response to gravity selection. Shortly after the evolution of clusters, the yeast evolved higher rates of cell death. While cell death enables clusters to split apart and form new groups, it also reduces their performance in the face of gravity selection. To understand the selective value of increased cell death, we create a mathematical model of the cellular arrangement within snowflake yeast clusters. The model reveals that the mechanism of cell death and the geometry of the snowflake interact in complex, evolutionarily important ways. We find that the organization of snowflake yeast imposes powerful limitations on the available space for new cell growth. By dying more frequently, cells in clusters avoid encountering space limitations, and, paradoxically, reach higher numbers. In addition, selection for particular group sizes can explain the increased rate of apoptosis both in terms of total cell number and total numbers of collectives. Thus, by considering the geometry of a primitive multicellular organism we can gain insight into the initial emergence of reproductive division of labor during an evolutionary transition in individuality.

Experimental evolution of multicellularity.

Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes.

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.

Genomic sequencing reveals convergent adaptation during experimental evolution in two budding yeast species.

Convergent evolution is central in the origins of multicellularity. Identifying the basis for convergent multicellular evolution is challenging because of the diverse evolutionary origins and environments involved. Haploid Kluyveromyces lactis populations evolve multicellularity during selection for increased settling in liquid media. Strong genomic and phenotypic convergence is observed between K. lactis and previously selected S. cerevisiae populations under similar selection, despite their >100-million-year divergence. We find K. lactis multicellularity is conferred by mutations in genes ACE2 or AIM44, with ACE2 being predominant. They are a subset of the six genes involved in the S. cerevisiae multicellularity. Both ACE2 and AIM44 regulate cell division, indicating that the genetic convergence is likely due to conserved cellular replication mechanisms. Complex population dynamics involving multiple ACE2/AIM44 genotypes are found in most K. lactis lineages. The results show common ancestry and natural selection shape convergence while chance and contingency determine the degree of divergence.

Detecting life by behavior, the overlooked sensitivity of behavioral assays.

Detecting life has driven research and exploration for centuries, but recent attempts to compile and generate a framework that summarizes life features, aimed to develop strategies for life detection missions beyond planet Earth, have disregarded a key life feature: behavior. Yet, some behaviors such as biomineralization or motility have occasionally been proposed as biosignatures to detect life. Here, we capitalize on a specific taxis' motility behavior, magnetotaxis, to experimentally provide insights in support of behavior as an unambiguous, sensitive biosignature, and magnetic forces as a prescreening option. Using a magnetotactic bacterial species, Magnetospirillum magneticum, we conducted a lab sensitivity experiment comparing PCR with the hanging drop behavioral assay, using a dilution series. The hanging drop behavioral assay visually shows the motility of MTB toward magnetic poles. Our findings reveal that the behavioral assay exhibits higher sensitivity in the detection of M. magneticum when compared to the established PCR protocol. While both methods present similar detection sensitivities at high concentrations, at ≥ 10-7 fold dilutions, the behavioral method proved more sensitive. The behavioral method can detect bacteria even when samples are diluted at 10-9. Comparable results were obtained with environmental samples from the Hula Valley. We propose behavioral cues as valuable biosignatures in the ongoing efforts of life detection in unexplored aquatic habitats on Earth and to stimulate and support discussions about how to detect extant life beyond Earth. Generic and robust behavioral assays can represent a methodological revolution.

Disentangling direct and indirect fitness effects of microbial dormancy.

Disentangling individual selection from kin selection is one of the greatest challenges of evolutionary biology. Even solitary organisms that do not interact directly with conspecifics may interact indirectly with them through competition for resources. As a result, traits that appear to affect individual fitness alone can also modify the fitness of relatives nearby and thus may evolve partially through these cryptic indirect fitness effects. Here we develop a method to quantitatively separate direct and indirect fitness consequences when some microbes become dormant, while neighbors of the same genotype remain active. Dormant microbes typically survive stresses that kill metabolically active cells, but dormancy also has a social side effect, sparing resources that may be used by nondormant individuals for growth. In structured populations, spared resources may be preferentially consumed by nondormant clonemates, providing an indirect benefit. Without population structure, however, exploitation by a never-dormant competitor imposes an indirect fitness cost on dormant cells. Cryptic indirect fitness effects may play a significant role in the evolution of many ostensibly asocial traits.

Season of conception in rural gambia affects DNA methylation at putative human metastable epialleles.

Throughout most of the mammalian genome, genetically regulated developmental programming establishes diverse yet predictable epigenetic states across differentiated cells and tissues. At metastable epialleles (MEs), conversely, epigenotype is established stochastically in the early embryo then maintained in differentiated lineages, resulting in dramatic and systemic interindividual variation in epigenetic regulation. In the mouse, maternal nutrition affects this process, with permanent phenotypic consequences for the offspring. MEs have not previously been identified in humans. Here, using an innovative 2-tissue parallel epigenomic screen, we identified putative MEs in the human genome. In autopsy samples, we showed that DNA methylation at these loci is highly correlated across tissues representing all 3 embryonic germ layer lineages. Monozygotic twin pairs exhibited substantial discordance in DNA methylation at these loci, suggesting that their epigenetic state is established stochastically. We then tested for persistent epigenetic effects of periconceptional nutrition in rural Gambians, who experience dramatic seasonal fluctuations in nutritional status. DNA methylation at MEs was elevated in individuals conceived during the nutritionally challenged rainy season, providing the first evidence of a permanent, systemic effect of periconceptional environment on human epigenotype. At MEs, epigenetic regulation in internal organs and tissues varies among individuals and can be deduced from peripheral blood DNA. MEs should therefore facilitate an improved understanding of the role of interindividual epigenetic variation in human disease.

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.

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.

Mesocosms of aquatic bacterial communities from the Cuatro Cienegas Basin (Mexico): a tool to test bacterial community response to environmental stress.

Microbial communities are responsible for important ecosystem processes, and their activities are regulated by environmental factors such as temperature and solar ultraviolet radiation. Here we investigate changes in aquatic microbial community structure, diversity, and evenness in response to changes in temperature and UV radiation. For this purpose, 15 mesocosms were seeded with both microbial mat communities and plankton from natural pools within the Cuatro Cienegas Basin (Mexico). Clone libraries (16S rRNA) were obtained from water samples at the beginning and at the end of the experiment (40 days). Phylogenetic analysis indicated substantial changes in aquatic community composition and structure in response to temperature and UV radiation. Extreme treatments with elevation in temperature or UV radiation reduced diversity in relation to the Control treatments, causing a reduction in richness and increase in dominance, with a proliferation of a few resistant operational taxonomic units. Each phylum was affected differentially by the new conditions, which translates in a differential modification of ecosystem functioning. This suggests that the impact of environmental stress, at least at short term, will reshape the aquatic bacterial communities of this unique ecosystem. This work also demonstrates the possibility of designing manageable synthetic microbial community ecosystems where controlled environmental variables can be manipulated. Therefore, microbial model systems offer a complementary approach to field and laboratory studies of global research problems associated with the environment.

Diversity of culturable thermo-resistant aquatic bacteria along an environmental gradient in Cuatro Ciénegas, Coahuila, México.

At the desert oasis of Cuatro Ciénegas in Coahuila, México, more than 300 oligotrophic pools can be found and a large number of endemic species of plants and animals. The most divergent taxa of diatoms, snail and fishes are located in the Churince hydrological system, where we analyzed the local diversification of cultivable Firmicutes and Actinobacteria. The Churince hydrological system is surrounded by gypsum dunes and has a strong gradient for salinity, temperature, pH and dissolved oxygen. In August 2003, surface water samples were taken in 10 sites along the Churince system together with the respective environmental measurements. 417 thermo-resistant bacteria were isolated and DNA was extracted to obtain their BOX-PCR fingerprints, revealing 55 different patterns. In order to identify similarities and differences in the diversity of the various sampling sites, an Ordination Analysis was applied using Principal Component Analysis. This analysis showed that conductivity is the environmental factor that explains the distribution of most of the microbial diversity. Phylogenetic reconstruction from their 16S rRNA sequences was performed for a sample of 150 isolates. Only 17 sequences had a 100% match in the Gene Bank (NCBI), representing 10 well known cosmopolitan taxa. The rest of the sequences cluster in 22 clades for Firmicutes and another 22 clades for Actinobacteria, supporting the idea of high diversity and differentiation for this site.

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.