MuLTEERatcliff Lab · Georgia Tech

Publications

Publications

Papers that use MuLTEE populations or material derived from them, followed by other key snowflake yeast work the experiment relies on. For the full lab publication list, see the Ratcliff Lab site.


Papers over time

Papers over time

Filled dots are MuLTEE papers, hollow dots are earlier snowflake yeast work. The amber line marks the first transfer, January 2018.

The interactive timeline needs JavaScript. Nothing is lost without it: every paper it plots appears in full, newest first, in the two lists below.

The right-hand edge is today's date.


MuLTEE

MuLTEE papers

  1. Emergence of coordinated cell division during the evolution of multicellularity

    Luis F. Cedeño-Pérez, Rozenn M. Pineau, Thomas C. Day, William C. Ratcliff, and Peter L. Conlin

    2025 PLOS Computational Biology In press Preprint: doi.org/10.1101/2025.04.23.650085

    The anaerobic MuLTEE ancestor divides asynchronously because daughter cells take about 25% longer for their first division, and this delay, not variance in doubling time, creates smaller, more branched clusters; synchronous division improves both growth rate and settling survival, and anaerobic MuLTEE populations had lost the first-division delay by day 200 and remained synchronous through day 1,000.

  2. Genome duplication in a long-term multicellularity evolution experiment

    Kai Tong, Sayantan Datta, Vivian Cheng, Daniella J. Haas, Saranya Gourisetti, Harley L. Yopp, Thomas C. Day, Dung T. Lac, Ahmad S. Khalil, Peter L. Conlin, G. Ozan Bozdag, and William C. Ratcliff

    2025 Nature 639:691–699 doi.org/10.1038/s41586-025-08689-6

    In all five mixotrophic and all five anaerobic MuLTEE populations, diploid snowflake yeast convergently became tetraploid by day 50 and fixed tetraploidy by day 100 because larger, longer tetraploid cells immediately produce larger clusters; tetraploidy was actively maintained by size-based selection for nearly 5,000 generations and opened downstream aneuploid routes to macroscopic size in the anaerobic lines.

  3. Real-time, high-throughput super-resolution microscopy via panoramic integration

    Kyungduck Yoon, Hansol Yoon, Kidan Tadesse, Zhi Ling, Biagio Mandracchia, Sayantan Datta, G. Ozan Bozdag, Anthony J. Burnetti, William C. Ratcliff, and Shu Jia

    2025 Nature Communications 16:9309 doi.org/10.1038/s41467-025-64368-0

    Super-resolution panoramic integration (SPI) achieves about twofold resolution improvement (point-spread function 152 ± 13 nm, improved to 116 ± 9 nm after Wiener-Butterworth deconvolution) while imaging up to 1.84 mm2/s, and applied to GFP-tagged ancestral and evolved anaerobic MuLTEE snowflake yeast it recovers the increase in cell aspect ratio from about 1.30 in ancestors to 3.28 by 1,000 transfers and module size growth from 30.7 µm to 87.1 µm.

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

    Nishant Narayanasamy, Emma Bingham, Tanner Fadero, G. Ozan Bozdag, William C. Ratcliff, Peter Yunker, and Shashi Thutupalli

    2025 Science Advances 11:eadr6399 doi.org/10.1126/sciadv.adr6399

    Millimetre-scale evolved anaerobic MuLTEE clusters keep growing exponentially in static liquid (but only sub-exponentially on agar) because metabolism generates persistent buoyancy-driven circulatory flows that advect nutrients through the porous entangled body; the flows vanish in dead or glucose-starved clusters, reverse with gravity, and appear only above a threshold cluster size.

  5. Morphological Entanglement in Living Systems

    Thomas C. Day, S. Alireza Zamani-Dahaj, G. Ozan Bozdag, Anthony J. Burnetti, Emma P. Bingham, Peter L. Conlin, William C. Ratcliff, and Peter J. Yunker

    2024 Physical Review X 14:011008 doi.org/10.1103/PhysRevX.14.011008

    Segmented 3D SEM reconstructions of evolved MuLTEE snowflake branches show branches caged by two or more neighbours that rigid-body translation and rotation cannot free, and simulations plus shaking-speed and budding-geometry experiments show that growth tunnels branching organisms into entangled states that agitation alone cannot access, making entanglement a timescale-limited rather than geometry-limited route to multicellular toughness.

  6. Proteostatic tuning underpins the evolution of novel multicellular traits

    Kristopher Montrose, Dung T. Lac, Anthony J. Burnetti, Kai Tong, G. Ozan Bozdag, Mikaela Hukkanen, William C. Ratcliff, and Juha Saarikangas

    2024 Science Advances 10:eadn2706 doi.org/10.1126/sciadv.adn2706

    All five anaerobic MuLTEE lineages that evolved macroscopic size convergently down-regulated the chaperone Hsp90 (HSC82), which destabilizes the cyclin-dependent kinase Cdc28, delays mitosis and prolongs polarized growth to elongate cells; reinstating Hsp90 or Cdc28 expression shortened cells, shrank clusters and reduced multicellular fitness.

  7. Emergence and maintenance of stable coexistence during a long-term multicellular evolution experiment

    Rozenn M. Pineau, Eric Libby, David Demory, Dung T. Lac, Thomas C. Day, Pablo Bravo, Peter J. Yunker, Joshua S. Weitz, G. Ozan Bozdag, and William C. Ratcliff

    2024 Nature Ecology & Evolution 8(5):1010–1020 doi.org/10.1038/s41559-024-02367-y

    Three of five obligately aerobic MuLTEE populations evolved stably coexisting small and large snowflake yeast lineages that persisted for nearly the full 4,300-generation experiment, maintained by negative frequency-dependent selection converging on roughly 9% Large and 91% Small, with oxygen competition during growth favouring small clusters and settling selection favouring large ones.

  8. De novo evolution of macroscopic multicellularity

    G. Ozan Bozdag, Seyed Alireza Zamani-Dahaj, Thomas C. Day, Penelope C. Kahn, Anthony J. Burnetti, Dung T. Lac, Kai Tong, Peter L. Conlin, Aishwarya H. Balwani, Eva L. Dyer, Peter J. Yunker, and William C. Ratcliff

    2023 Nature 617:747–754 doi.org/10.1038/s41586-023-06052-1

    After 600 rounds of daily growth-plus-settling selection, all five anaerobic MuLTEE populations evolved millimetre-scale clonal bodies, increasing mean cluster radius from 16 µm to 434 µm (roughly 2 × 104 times larger by volume) and becoming about 104-fold biophysically tougher through cell elongation and branch entanglement, while snowflake yeast competing for low oxygen remained microscopic and evolved to be only about sixfold larger.

  9. Oxygen suppression of macroscopic multicellularity

    G. Ozan Bozdag, Eric Libby, Rozenn Pineau, Christopher T. Reinhard, and William C. Ratcliff

    2021 Nature Communications 12:2838 doi.org/10.1038/s41467-021-23104-0

    Across roughly 812 generations of settling selection in 20 populations under four oxygen and metabolic regimes, anaerobic and high-oxygen snowflake yeast increased mean size by 93% and 97% respectively while strictly aerobic yeast at intermediate oxygen increased only 8.9%, with cellular aspect ratio explaining 92% of the variation in cluster size. These twenty populations were founded in 2018, and fifteen of them have been transferred daily ever since. This is the experiment that became the MuLTEE.


Snowflake yeast

Other key work relevant to the MuLTEE

  1. Oxygen-binding proteins aid oxygen diffusion to enhance fitness of a yeast model of multicellularity

    Whitney Wong, Pablo Bravo, Peter J. Yunker, William C. Ratcliff, Anthony J. Burnetti

    2025 PLOS Biology 23(1): e3002975 doi.org/10.1371/journal.pbio.3002975

    Heterologously expressed sperm whale myoglobin and peanut worm myohemerythrin increased mean oxygen diffusion depth in snowflake yeast clusters from 16 µm to 21 µm under low oxygen, and the fitness advantage was 2.6-fold (myohemerythrin) and 1.9-fold (myoglobin) larger under supplemental oxygen than under low oxygen, with no detectable benefit for small bud8Δ clusters.

  2. Cellular packing, mechanical stress and the evolution of multicellularity

    Shane Jacobeen, Jennifer T. Pentz, Elyes C. Graba, Colin G. Brandys, William C. Ratcliff, Peter J. Yunker

    2018 Nature Physics 14, 286–290 doi.org/10.1038/s41567-017-0002-y

    Snowflake yeast clusters fracture from crowding-induced internal stress rather than bond weakness, and over seven weeks (roughly 291 generations) of size selection clusters increased average radius 1.7-fold by evolving an 8% larger cell aspect ratio that dropped cluster volume fraction from 0.32 ± 0.04 to 0.22 ± 0.03, while chitin bond size did not change.

  3. Geometry, packing, and evolutionary paths to increased multicellular size

    Shane Jacobeen, Elyes C. Graba, Colin G. Brandys, T. Cooper Day, William C. Ratcliff, Peter J. Yunker

    2018 Physical Review E 97(5): 050401 doi.org/10.1103/PhysRevE.97.050401

    In a validated geometric model of snowflake yeast, increasing cellular aspect ratio is always a more efficient route to larger size than strengthening intercellular bonds, adding on average about 13 times more cells per equal parameter increment (about 59 times for spherical cells), with cluster size maximized near a 54 degree attachment angle.

  4. Origins of Multicellular Evolvability in Snowflake Yeast

    William C. Ratcliff, Johnathon D. Fankhauser, David W. Rogers, Duncan Greig, Michael Travisano

    2015 Nature Communications 6: 6102 doi.org/10.1038/ncomms7102

    Disruption of the transcription factor ACE2 is sufficient to produce the snowflake phenotype (non-synonymous ACE2 mutations in 5 of 10 independently evolved lineages; ACE2 knockout creates clusters, complementation restores unicellularity), and the resulting clonal branching growth form follows Pascal's triangle and yields broad-sense heritability of H2 = 0.84 for cluster size at reproduction.

  5. Geometry Shapes Evolution of Early Multicellularity

    Eric Libby, William Ratcliff, Michael Travisano, Ben Kerr

    2014 PLoS Computational Biology 10(9): e1003803 doi.org/10.1371/journal.pcbi.1003803

    A mathematical model of snowflake cluster geometry shows that the branching tree topology imposes interior space constraints, so elevated cell death is paradoxically adaptive: in simulated populations the probability of cell death rises from 10−8 to about 10−2 within roughly 60 transfers, matching the experimental observation.

  6. Tempo and Mode of Multicellular Adaptation in Experimentally Evolved Saccharomyces cerevisiae

    William C. Ratcliff, Jennifer T. Pentz, and Michael Travisano

    2013 Evolution 67: 1573–1581 doi.org/10.1111/evo.12101

    Over 227 days settling speed increased 44% through three temporally distinct phases: more cells per cluster (42.6 at day 7 to 114.5 at day 227), then a 2.21-fold increase in cell volume, then rounder, more hydrodynamic clusters (5.7% more round at day 227 than day 65).

  7. Experimental Evolution of Multicellularity

    William C. Ratcliff, R. Ford Denison, Mark Borrello, Michael Travisano

    2012 Proceedings of the National Academy of Sciences 109(5), 1595–1600 doi.org/10.1073/pnas.1115323109

    All 10 replicate populations evolved clonal multicellular snowflake clusters within 60 transfers of gravity-based settling selection, displaying a novel multicellular life history with a juvenile phase, propagules consistently less than half the parent cluster size, and rudimentary division of labor via evolved apoptosis.