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Partner fidelity and coevolution: Useful but not required for rapidly increased mutualistic benefitsAbstract Evolutionary theory predicts that specialization between mutualistic partners is beneficial, limiting conflict and increasing the opportunity to evolve cooperative benefits through sustained reciprocal selection. However, specialized mutualisms are relatively rare in nature. Few empirical studies have directly examined how multi-partner interactions affect mutualistic evolution, largely because tracking partner dynamics over evolutionary timescales is challenging in natural systems. We circumvent this constraint via experimental evolution with an engineered resource sharing mutualism in Baker’s yeast (Saccharomyces cerevisiae), which allows precise control of partner fidelity across generations. We compared high partner fidelity (consistent pairings) with low partner fidelity (temporally rotating partners) across 54 rounds of selection. High partner fidelity produced the strongest mutualistic benefits (7.2% increased growth over controls), while low partner fidelity yielded only modest benefits (2.2% increase). Time-shift experiments confirmed that while coevolution enhanced benefit evolution, it was not strictly necessary: benefits also evolved through one-sided adaptation. Genomic analyses revealed parallel evolution in amino acid metabolism and starvation response genes, with the slower-growing genotype driving most evolutionary change. Surprisingly, high-fidelity lineages evolved as generalists rather than specialists, cooperating equally well with all partners tested. Overall, these results demonstrate that partner fidelity facilitates the rapid evolution of mutualistic benefits but is not strictly required for mutualistic evolution.more » « lessFree, publicly-accessible full text available September 8, 2026
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The ecological and evolutionary success of multicellular lineages stems substantially from their increased size relative to unicellular ancestors. However, large size poses biophysical challenges, especially regarding nutrient transport: These constraints are typically overcome through multicellular innovations. 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. 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 ciliary actuation in extant multicellular organisms. These flows support exponential growth at macroscopic sizes that theory predicts should be diffusion limited. This demonstrates how simple physical mechanisms can act as a “biophysical scaffold” to support the evolution of multicellularity by opening up phenotypic possibilities before genetically encoded innovations.more » « less
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Abstract ‘Complex’ multicellularity has evolved in just five lineages (animals, plants, brown algae, red algae, and fungi) and in each case, these organisms develop clonally and are obligately multicellular. While prior work has shown that clonal development plays a critical role in the evolution of complex multicellularity, none has disentangled this from the impact of obligate vs facultative multicellular life cycles. Here we use experimental evolution with engineered ‘snowflake yeast’ (Saccharomyces cerevisiae) to directly test how life cycle structure affects multicellular adaptation. We created isogenic strains capable of switching between unicellular and clonal multicellular phases, then evolved populations for 192 days under obligately multicellular, facultatively multicellular, and obligately unicellular regimes. Obligately multicellular populations rapidly evolved larger size, primarily driven by a whole genome duplication, in all five replicates. Facultative populations showed dramatically constrained evolution, with tetraploidy evolving in only 2/10 facultative populations despite experiments demonstrating that it is strongly beneficial across the full life cycle. Mathematical modeling reveals the mechanistic basis for this constraint: facultative life cycles create establishment barriers through two population genetic effects. Group formation dramatically reduces the number of units of selection, making beneficial multicellular mutations vulnerable to drift. This asymmetry in population size between life cycle phases also allows cell-level selection to overpower group-level selection, eliminating mutations that provide group-level benefits but carry cell-level costs. These findings demonstrate that obligate multicellularity circumvents fundamental population genetic barriers to collective-level adaptation, helping explain why complex multicellularity has evolved exclusively in obligately multicellular lineages, and suggesting similar constraints may operate in other evolutionary transitions in individuality.more » « lessFree, publicly-accessible full text available May 15, 2027
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Free, publicly-accessible full text available December 1, 2026
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Abstract Ferro-rotational magnet RbFe(SO4)2has attracted attention for its stable ferro-rotational phase and electric-field-controlled magnetic chirality. This work presents the multiferroic properties andH–Tphase diagram of RbFe(SO4)2, which have been underexplored. Our measurements of magnetic susceptibility, ferroelectric polarization, and dielectric constant under various magnetic fields reveal four distinct phases: (I) a ferroelectric and helical magnetic phase below 4 K and 6 T, (II) a paraelectric and collinear magnetic phase below 4 K and above 6 T, (III) a paraelectric and non-collinear magnetic phase below 4 K and above 9 T, and (IV) a paraelectric and paramagnetic above 4 K. This study clarifies the multiferroic behavior andH–Tphase diagram of RbFe(SO4)2, providing valuable insights into ferro-rotational magnets.more » « less
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Abstract The evolutionary transition to multicellularity requires shifting the primary unit of selection from cells to multicellular collectives. How this occurs in aggregative organisms remains poorly understood. Clonal development provides a direct path to multicellular adaptation through genetic identity between cells, but aggregative organisms face a constraint: selection on collective-level traits cannot drive adaptation without positive genetic assortment. We leveraged experimental evolution of flocculatingSaccharomyces cerevisiaeto examine the evolution and role of genetic assortment in multicellular adaptation. After 840 generations of selection for rapid settling, 13 of 19 lineages evolved increased positive assortment relative to their ancestor. However, assortment provided no competitive advantage during settling selection, suggesting it arose as an indirect effect of selection on cell-level traits rather than through direct selection on collective-level properties. Genetic reconstruction experiments and protein structure modeling revealed two distinct pathways to assortment: kin recognition mediated by mutations in theFLO1adhesion gene and generally enhanced cellular adhesion that improved flocculation efficiency independent of partner genotype. The evolution of assortment without immediate adaptive benefit suggests that key innovations enabling multicellular adaptation may arise indirectly through cell-level selection. Our results demonstrate fundamental constraints on aggregative multicellularity and help explain why aggregative lineages have remained simple.more » « less
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Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularityShou, Wenying (Ed.)Oxygen availability is a key factor in the evolution of multicellularity, as larger and more sophisticated organisms often require mechanisms allowing efficient oxygen delivery to their tissues. One such mechanism is the presence of oxygen-binding proteins, such as globins and hemerythrins, which arose in the ancestor of bilaterian animals. Despite their importance, the precise mechanisms by which oxygen-binding proteins influenced the early stages of multicellular evolution under varying environmental oxygen levels are not yet clear. We address this knowledge gap by heterologously expressing the oxygen-binding proteins myoglobin and myohemerythrin in snowflake yeast, a model system of simple, undifferentiated multicellularity. These proteins increased the depth and rate of oxygen diffusion, increasing the fitness of snowflake yeast growing aerobically. Experiments show that, paradoxically, oxygen-binding proteins confer a greater fitness benefit for larger organisms when O2is least limiting. We show via biophysical modeling that this is because facilitated diffusion is more efficient when oxygen is abundant, transporting a greater quantity of O2which can be used for metabolism. By alleviating anatomical diffusion limitations to oxygen consumption, the evolution of oxygen-binding proteins in the oxygen-rich Neoproterozoic may have been a key breakthrough enabling the evolution of increasingly large, complex multicellular metazoan lineages.more » « less
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