De novo evolution of macroscopic multicellularity.

While early multicellular lineages necessarily started out as relatively simple groups of cells, little is known about how they became Darwinian entities capable of sustained multicellular evolution1-3. Here we investigate this with a multicellularity long-term evolution experiment, selecting for larger group size in the snowflake yeast (Saccharomyces cerevisiae) model system. Given the historical importance of oxygen limitation4, our ongoing experiment consists of three metabolic treatments5-anaerobic, obligately aerobic and mixotrophic yeast. After 600 rounds of selection, snowflake yeast in the anaerobic treatment group evolved to be macroscopic, becoming around 2 × 104 times larger (approximately mm scale) and about 104-fold more biophysically tough, while retaining a clonal multicellular life cycle. This occurred through biophysical adaptation-evolution of increasingly elongate cells that initially reduced the strain of cellular packing and then facilitated branch entanglements that enabled groups of cells to stay together even after many cellular bonds fracture. By contrast, snowflake yeast competing for low oxygen5 remained microscopic, evolving to be only around sixfold larger, underscoring the critical role of oxygen levels in the evolution of multicellular size. Together, this research provides unique insights into an ongoing evolutionary transition in individuality, showing how simple groups of cells overcome fundamental biophysical limitations through gradual, yet sustained, multicellular evolution.

Uncovering the hidden complexity of multicellular magnetotactic bacteria.

Multicellular magnetotactic bacteria (MMB) have a surprisingly complex multicellular lifestyle. A new study in PLOS Biology combines genomics, microscopy, and isotopic labeling to show that MMB form obligately multicellular consortia of genetically diverse cells with rudimentary division of labor.

A nonadaptive explanation for macroevolutionary patterns in the evolution of complex multicellularity.

"Complex multicellularity," conventionally defined as large organisms with many specialized cell types, has evolved five times independently in eukaryotes, but never within prokaryotes. A number of hypotheses have been proposed to explain this phenomenon, most of which posit that eukaryotes evolved key traits (e.g., dynamic cytoskeletons, alternative mechanisms of gene regulation, or subcellular compartments) which were a necessary prerequisite for the evolution of complex multicellularity. Here, we propose an alternative, nonadaptive hypothesis for this broad macroevolutionary pattern. By binning cells into groups with finite genetic bottlenecks between generations, the evolution of multicellularity greatly reduces the effective population size (Ne) of cellular populations, increasing the role of genetic drift in evolutionary change. While both prokaryotes and eukaryotes experience this phenomenon, they have opposite responses to drift: eukaryotes tend to undergo genomic expansion, providing additional raw genetic material for subsequent multicellular innovation, while prokaryotes generally face genomic erosion. Taken together, we hypothesize that these idiosyncratic lineage-specific evolutionary dynamics play a fundamental role in the long-term divergent evolution of complex multicellularity across the tree of life.

Experimental evolution is not just for model organisms.

In a new paper published in PLOS Biology, Dudin and colleagues evolve simple multicellularity in Sphaeroforma arctica, a unicellular relative of animals. This work establishes a new and open-ended avenue for examining the evolution of multicellularity in an important but understudied group of organisms.

Atomically engineered ferroic layers yield a room-temperature magnetoelectric multiferroic.

Materials that exhibit simultaneous order in their electric and magnetic ground states hold promise for use in next-generation memory devices in which electric fields control magnetism. Such materials are exceedingly rare, however, owing to competing requirements for displacive ferroelectricity and magnetism. Despite the recent identification of several new multiferroic materials and magnetoelectric coupling mechanisms, known single-phase multiferroics remain limited by antiferromagnetic or weak ferromagnetic alignments, by a lack of coupling between the order parameters, or by having properties that emerge only well below room temperature, precluding device applications. Here we present a methodology for constructing single-phase multiferroic materials in which ferroelectricity and strong magnetic ordering are coupled near room temperature. Starting with hexagonal LuFeO3-the geometric ferroelectric with the greatest known planar rumpling-we introduce individual monolayers of FeO during growth to construct formula-unit-thick syntactic layers of ferrimagnetic LuFe2O4 (refs 17, 18) within the LuFeO3 matrix, that is, (LuFeO3)m/(LuFe2O4)1 superlattices. The severe rumpling imposed by the neighbouring LuFeO3 drives the ferrimagnetic LuFe2O4 into a simultaneously ferroelectric state, while also reducing the LuFe2O4 spin frustration. This increases the magnetic transition temperature substantially-from 240 kelvin for LuFe2O4 (ref. 18) to 281 kelvin for (LuFeO3)9/(LuFe2O4)1. Moreover, the ferroelectric order couples to the ferrimagnetism, enabling direct electric-field control of magnetism at 200 kelvin. Our results demonstrate a design methodology for creating higher-temperature magnetoelectric multiferroics by exploiting a combination of geometric frustration, lattice distortions and epitaxial engineering.

Why have aggregative multicellular organisms stayed simple?

Multicellularity has evolved numerous times across the tree of life. One of the most fundamental distinctions among multicellular organisms is their developmental mode: whether they stay together during growth and develop clonally, or form a group through the aggregation of free-living cells. The five eukaryotic lineages to independently evolve complex multicellularity (animals, plants, red algae, brown algae, and fungi) all develop clonally. This fact has largely been explained through social evolutionary theory's lens of cooperation and conflict, where cheating within non-clonal groups has the potential to undermine multicellular adaptation. Multicellular organisms that form groups via aggregation could mitigate the costs of cheating by evolving kin recognition systems that prevent the formation of chimeric groups. However, recent work suggests that selection for the ability to aggregate quickly may constrain the evolution of highly specific kin recognition, sowing the seeds for persistent evolutionary conflict. Importantly, other features of aggregative multicellular life cycles may independently act to constrain the evolution of complex multicellularity. All known aggregative multicellular organisms are facultatively multicellular (as opposed to obligately multicellular), allowing unicellular-level adaptation to environmental selection. Because they primarily exist in a unicellular state, it may be difficult for aggregative multicellular organisms to evolve multicellular traits that carry pleiotropic cell-level fitness costs. Thus, even in the absence of social conflict, aggregative multicellular organisms may have limited potential for the evolution of complex multicellularity.

Shortsighted Evolution Constrains the Efficacy of Long-Term Bet Hedging.

To survive unpredictable environmental change, many organisms adopt bet-hedging strategies that are initially costly but provide a long-term fitness benefit. The temporal extent of these deferred fitness benefits determines whether bet-hedging organisms can survive long enough to realize them. In this article, we examine a model of microbial bet hedging in which there are two paths to extinction: unpredictable environmental change and demographic stochasticity. In temporally correlated environments, these drivers of extinction select for different switching strategies. Rapid phenotype switching ensures survival in the face of unpredictable environmental change, while slower-switching organisms become extinct. However, when both switching strategies are present in the same population, then demographic stochasticity-enforced by a limited population size-leads to extinction of the faster-switching organism. As a result, we find a novel form of evolutionary suicide whereby selection in a fluctuating environment can favor bet-hedging strategies that ultimately increase the risk of extinction. Population structures with multiple subpopulations and dispersal can reduce the risk of extinction from unpredictable environmental change and shift the balance so as to facilitate the evolution of slower-switching organisms.

An oscillating tragedy of the commons in replicator dynamics with game-environment feedback.

A tragedy of the commons occurs when individuals take actions to maximize their payoffs even as their combined payoff is less than the global maximum had the players coordinated. The originating example is that of overgrazing of common pasture lands. In game-theoretic treatments of this example, there is rarely consideration of how individual behavior subsequently modifies the commons and associated payoffs. Here, we generalize evolutionary game theory by proposing a class of replicator dynamics with feedback-evolving games in which environment-dependent payoffs and strategies coevolve. We initially apply our formulation to a system in which the payoffs favor unilateral defection and cooperation, given replete and depleted environments, respectively. Using this approach, we identify and characterize a class of dynamics: an oscillatory tragedy of the commons in which the system cycles between deplete and replete environmental states and cooperation and defection behavior states. We generalize the approach to consider outcomes given all possible rational choices of individual behavior in the depleted state when defection is favored in the replete state. In so doing, we find that incentivizing cooperation when others defect in the depleted state is necessary to avert the tragedy of the commons. In closing, we propose directions for the study of control and influence in games in which individual actions exert a substantive effect on the environmental state.

Trait heritability in major transitions.

BACKGROUND: Increases in biological complexity and the origins of life's hierarchical organization are described by the "major transitions" framework. A crucial component of this paradigm is that after the transition in complexity or organization, adaptation occurs primarily at the level of the new, higher-level unit. For collective-level adaptations to occur, though, collective-level traits-properties of the group, such as collective size-must be heritable. Since collective-level trait values are functions of lower-level trait values, collective-level heritability is related to particle-level heritability. However, the nature of this relationship has rarely been explored in the context of major transitions. RESULTS: We examine relationships between particle-level heritability and collective-level heritability for several functions that express collective-level trait values in terms of particle-level trait values. For clonal populations, when a collective-level trait value is a linear function of particle-level trait values and the number of particles per collective is fixed, the heritability of a collective-level trait is never less than that of the corresponding particle-level trait and is higher under most conditions. For more complicated functions, collective-level heritability is higher under most conditions, but can be lower when the environment experienced by collectives is heterogeneous. Within-genotype variation in collective size reduces collective-level heritability, but it can still exceed particle-level heritability when phenotypic variance among particles within collectives is large. These results hold for a diverse sample of biologically relevant traits. CONCLUSIONS: Rather than being an impediment to major transitions, we show that, under a wide range of conditions, the heritability of collective-level traits is actually higher than that of the corresponding particle-level traits. High levels of collective-level trait heritability thus arise "for free," with important implications not only for major transitions but for multilevel selection in general.

Electric-Field Induced Reversible Switching of the Magnetic Easy Axis in Co/BiFeO3 on SrTiO3.

Electric-field (E-field) control of magnetism enabled by multiferroic materials has the potential to revolutionize the landscape of present memory devices plagued with high energy dissipation. To date, this E-field controlled multiferroic scheme has only been demonstrated at room temperature using BiFeO3 films grown on DyScO3, a unique and expensive substrate, which gives rise to a particular ferroelectric domain pattern in BiFeO3. Here, we demonstrate reversible electric-field-induced switching of the magnetic state of the Co layer in Co/BiFeO3 (BFO) (001) thin film heterostructures fabricated on (001) SrTiO3 (STO) substrates. The angular dependence of the coercivity and the remanent magnetization of the Co layer indicates that its easy axis reversibly switches back and forth 45° between the (100) and the (110) crystallographic directions of STO as a result of alternating application of positive and negative voltage pulses between the patterned top Co electrode layer and the (001) SrRuO3 (SRO) layer on which the ferroelectric BFO is epitaxially grown. The coercivity (HC) of the Co layer exhibits a hysteretic behavior between two states as a function of voltage. A mechanism based on the intrinsic magnetoelectric coupling in multiferroic BFO involving projection of antiferromagnetic G-type domains is used to explain the observation. We have also measured the exact canting angle of the G-type domain in strained BFO films for the first time using neutron diffraction. These results suggest a pathway to integrating BFO-based devices on Si wafers for implementing low power consumption and nonvolatile magnetoelectronic devices.

Magnetic structure and ordering of multiferroic hexagonal LuFeO_{3}.

We report on the magnetic structure and ordering of hexagonal LuFeO_{3} films of variable thickness grown by molecular-beam epitaxy on YSZ (111) and Al_{2}O_{3} (0001) substrates. These crystalline films exhibit long-range structural uniformity dominated by the polar P6_{3}cm phase, which is responsible for the paraelectric to ferroelectric transition that occurs above 1000 K. Using bulk magnetometry and neutron diffraction, we find that the system orders into a ferromagnetically canted antiferromagnetic state via a single transition below 155 K regardless of film thickness, which is substantially lower than that previously reported in hexagonal LuFeO_{3} films. The symmetry of the magnetic structure in the ferroelectric state implies that this material is a strong candidate for linear magnetoelectric coupling and control of the ferromagnetic moment directly by an electric field.

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.

Transforming yeast into a facultative photoheterotroph via expression of vacuolar rhodopsin.

Phototrophic metabolism, the capture of light for energy, was a pivotal biological innovation that greatly increased the total energy available to the biosphere. Chlorophyll-based photosynthesis is the most familiar phototrophic metabolism, but retinal-based microbial rhodopsins transduce nearly as much light energy as chlorophyll does,1 via a simpler mechanism, and are found in far more taxonomic groups. Although this system has apparently spread widely via horizontal gene transfer,2,3,4 little is known about how rhodopsin genes (with phylogenetic origins within prokaryotes5,6) are horizontally acquired by eukaryotic cells with complex internal membrane architectures or the conditions under which they provide a fitness advantage. To address this knowledge gap, we sought to determine whether Saccharomyces cerevisiae, a heterotrophic yeast with no known evolutionary history of phototrophy, can function as a facultative photoheterotroph after acquiring a single rhodopsin gene. We inserted a rhodopsin gene from Ustilago maydis,7 which encodes a proton pump localized to the vacuole, an organelle normally acidified via a V-type rotary ATPase, allowing the rhodopsin to supplement heterotrophic metabolism. Probes of the physiology of modified cells show that they can deacidify the cytoplasm using light energy, demonstrating the ability of rhodopsins to ameliorate the effects of starvation and quiescence. Further, we show that yeast-bearing rhodopsins gain a selective advantage when illuminated, proliferating more rapidly than their non-phototrophic ancestor or rhodopsin-bearing yeast cultured in the dark. These results underscore the ease with which rhodopsins may be horizontally transferred even in eukaryotes, providing novel biological function without first requiring evolutionary optimization.

Constitutive expression of the Type VI Secretion System carries no measurable fitness cost in Vibrio cholerae.

The Type VI Secretion System (T6SS) is a widespread and highly effective mechanism of microbial warfare; it confers the ability to efficiently kill susceptible cells within close proximity. Due to its large physical size, complexity, and ballistic basis for intoxication, it has widely been assumed to incur significant growth costs in the absence of improved competitive outcomes. In this study, we precisely examine the fitness costs of constitutive T6SS firing in the bacterium Vibrio cholerae. We find that, contrary to expectations, constitutive expression of the T6SS has a negligible impact on growth, reducing growth fitness by 0.025 ± 0.5% (95% CI) relative to a T6SS- control. Mathematical modeling of microbial populations demonstrates that, due to clonal interference, constitutive expression of the T6SS will often be neutral, with little impact on evolutionary outcomes. Our findings underscore the importance of precisely measuring the fitness costs of microbial social behaviors and help explain the prevalence of the T6SS across Gram-negative bacteria.

Metabolically-driven flows enable exponential growth in macroscopic multicellular yeast.

The ecological and evolutionary success of multicellular lineages is due in no small part to their increased size relative to unicellular ancestors. However, large size also poses biophysical challenges, especially regarding the transport of nutrients to all cells; these constraints are typically overcome through multicellular innovations (e.g., a circulatory system). Here we show that an emergent biophysical mechanism - spontaneous fluid flows arising from metabolically-generated density gradients - can alleviate constraints on nutrient transport, enabling exponential growth in nascent multicellular clusters of yeast lacking any multicellular adaptations for nutrient transport or fluid flow. Surprisingly, beyond a threshold size, the metabolic activity of experimentally-evolved snowflake yeast clusters drives large-scale fluid flows that transport nutrients throughout the cluster at speeds comparable to those generated by the cilia of extant multicellular organisms. These flows support exponential growth at macroscopic sizes that theory predicts should be diffusion limited. This work demonstrates how simple physical mechanisms can act as a 'biophysical scaffold' to support the evolution of multicellularity by opening up phenotypic possibilities prior to genetically-encoded innovations. More broadly, our findings highlight how co-option of conserved physical processes is a crucial but underappreciated facet of evolutionary innovation across scales.

Proteostatic tuning underpins the evolution of novel multicellular traits.

The evolution of multicellularity paved the way for the origin of complex life on Earth, but little is known about the mechanistic basis of early multicellular evolution. Here, we examine the molecular basis of multicellular adaptation in the Multicellularity Long Term Evolution Experiment (MuLTEE). We demonstrate that cellular elongation, a key adaptation underpinning increased biophysical toughness and organismal size, is convergently driven by downregulation of the chaperone Hsp90. Mechanistically, Hsp90-mediated morphogenesis operates by destabilizing the cyclin-dependent kinase Cdc28, resulting in delayed mitosis and prolonged polarized growth. Reinstatement of Hsp90 or Cdc28 expression resulted in shortened cells that formed smaller groups with reduced multicellular fitness. Together, our results show how ancient protein folding systems can be tuned to drive rapid evolution at a new level of biological individuality by revealing novel developmental phenotypes.

Proteostatic tuning underpins the evolution of novel multicellular traits.

The evolution of multicellularity paved the way for the origin of complex life on Earth, but little is known about the mechanistic basis of early multicellular evolution. Here, we examine the molecular basis of multicellular adaptation in the multicellularity long-term evolution experiment (MuLTEE). We demonstrate that cellular elongation, a key adaptation underpinning increased biophysical toughness and organismal size, is convergently driven by down-regulation of the chaperone Hsp90. Mechanistically, Hsp90-mediated morphogenesis operates by destabilizing the cyclin-dependent kinase Cdc28, resulting in delayed mitosis and prolonged polarized growth. Reinstatement of Hsp90 or Cdc28 expression resulted in shortened cells that formed smaller groups with reduced multicellular fitness. Together, our results show how ancient protein folding systems can be tuned to drive rapid evolution at a new level of biological individuality by revealing novel developmental phenotypes.

Electric-Field Manipulation of Magnetic Chirality in a Homo-Ferro-Rotational Helimagnet.

Ferro-rotational (FR) materials, renowned for their distinctive material functionalities, present challenges in the growth of homo-FR crystals (i.e., single FR domain). This study explores a cost-effective approach to growing homo-FR helimagnetic RbFe(SO4)2 (RFSO) crystals by lowering the crystal growth temperature below the TFR threshold using the high-pressure hydrothermal method. Through polarized neutron diffraction experiments, it is observed that nearly 86% of RFSO crystals consist of a homo-FR domain. Notably, RFSO displays remarkable stability in the FR phase, with an exceptionally high TFR of ≈573 K. Furthermore, RFSO exhibits a chiral helical magnetic structure with switchable ferroelectric polarization below 4 K. Importantly, external electric fields can induce a single magnetic domain state and manipulate its magnetic chirality. The findings suggest that the search for new FR magnets with outstanding material properties should consider magnetic sulfates as promising candidates.