Collaborative research: Origin of multicellular complexity in experimentally-evolved Saccharomyces cerevisiae

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How did complex multicellular life arise from the single-celled microorganisms that defined life on Earth for billions of years? The rise of multicellular organisms drove a profound diversification of life that fundamentally changed Earth's ecology, yet little is known about how this major evolutionary transition occurred. This is largely due to the fact that most multicellular lineages are ancient, and early steps in this transition have been obscured by extinction. The PIs have overcome this limitation by developing a novel laboratory system, experimentally evolving simple multicellularity in Baker's yeast. Over thousands of generations of laboratory evolution, these cluster-forming 'snowflake yeast' evolve a suite of multicellular adaptations, including larger cluster size, an elevated rate of programmed cell death, and a more hydrodynamic profile. The PIs will use this model system to examine how novel multicellular traits arise in evolution, and will determine whether a fundamental developmental mechanism, the single-celled bottleneck that most multicellular organisms pass through (e.g., a single fertilized egg), improves the ability of natural selection to act on these emergent multicellular traits. This interdisciplinary work utilizes cutting-edge techniques in experimental evolution, next generation sequencing, molecular genetics, confocal microscopy, image analysis, and mathematical modeling. By illuminating the earliest steps in the evolutionary transition to multicellularity, the proposed research will help resolve an outstanding problem of central importance to biology. The evolution of biological complexity remains challenging to teach, particularly at the high school level. This award will support the development of a novel lab module, suitable for both high school and college classes, in which students use snowflake yeast and computer simulations to examine the evolution of multicellularity. The PIs will hold summer on-campus workshops to train teachers in the Atlanta area to use this curricula.Recent experiments have shown that unicellular organisms readily evolve to form multi-celled clusters, but little is known about how cellular clusters subsequently evolve greater multicellular complexity. The proposed research addresses this subject directly by asking the following questions: How do multicellular traits arise in evolution when mutation and recombination can only directly affect cell-level phenotype? Can early developmental mechanisms evolve to facilitate selection on these emergent multicellular traits? How are genes recruited for developmental functionality, and how are novel multicellular adaptations integrated into overall organism form and function? Answering the above questions will provide fundamental insight into the evolutionary origins of multicellular complexity, and will provide a theoretical foundation for similar investigations in other major evolutionary transitions. Snowflake yeast are an ideal experimental system for this work: the PIs have already evolved substantial morphological novelty, the snowflake growth form is mathematically tractable and has already been modeled by the PIs, and the extensive bioinformatic and molecular genetic tools developed for yeast allows for synthetic construction of multicellular strains with precisely defined properties.