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De novo evolution of macroscopic multicellularity

View ORCID ProfileG. Ozan Bozdag, Seyed Alireza Zamani-Dahaj, Penelope C. Kahn, Thomas C. Day, Kai Tong, Aishwarya H. Balwani, Eva L. Dyer, View ORCID ProfilePeter J. Yunker, William C. Ratcliff
doi: https://doi.org/10.1101/2021.08.03.454982
G. Ozan Bozdag
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA
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  • For correspondence: ozan.bozdag@gmail.com ratcliff@gatech.edu peter.yunker@gatech.edu
Seyed Alireza Zamani-Dahaj
2Interdisciplinary Graduate Program in Quantitative Biosciences, Georgia Institute of Technology, Atlanta, GA, USA
3School of Physics, Georgia Institute of Technology, Atlanta, GA, USA
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Penelope C. Kahn
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA
4Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada
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Thomas C. Day
3School of Physics, Georgia Institute of Technology, Atlanta, GA, USA
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Kai Tong
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA
2Interdisciplinary Graduate Program in Quantitative Biosciences, Georgia Institute of Technology, Atlanta, GA, USA
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Aishwarya H. Balwani
5School of Electrical & Computer Engineering, Georgia Institute of Technology, Atlanta, GA, USA
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Eva L. Dyer
5School of Electrical & Computer Engineering, Georgia Institute of Technology, Atlanta, GA, USA
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Peter J. Yunker
2Interdisciplinary Graduate Program in Quantitative Biosciences, Georgia Institute of Technology, Atlanta, GA, USA
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  • ORCID record for Peter J. Yunker
  • For correspondence: ozan.bozdag@gmail.com ratcliff@gatech.edu peter.yunker@gatech.edu
William C. Ratcliff
1School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA, USA
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  • For correspondence: ozan.bozdag@gmail.com ratcliff@gatech.edu peter.yunker@gatech.edu
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Abstract

The evolution of large organismal size is fundamentally important for multicellularity, creating new ecological niches and opportunities for the evolution of increased biological complexity. Yet little is known about how large size evolves, particularly in nascent multicellular organisms that lack genetically-regulated multicellular development. Here we examine the interplay between biological and biophysical drivers of macroscopic multicellularity using long-term experimental evolution. Over 600 daily transfers (~3,000 generations), multicellular snowflake yeast evolved macroscopic size, becoming ~2·104 times larger (~mm scale) and 104-fold more biophysically tough, while remaining clonal. They accomplished this through sustained biophysical adaptation, evolving increasingly elongate cells that initially reduced the strain of cellular packing, then facilitated branch entanglement so that groups of cells stay together even after many cellular bonds fracture. Four out of five replicate populations show evidence of predominantly adaptive evolution, with mutations becoming significantly enriched in genes affecting cell shape and cell-cell bonds. Taken together, this work shows how selection acting on the emergent properties of simple multicellular groups can drive sustained biophysical adaptation, an early step in the evolution of increasingly complex multicellular organisms.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 05, 2021.
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De novo evolution of macroscopic multicellularity
G. Ozan Bozdag, Seyed Alireza Zamani-Dahaj, Penelope C. Kahn, Thomas C. Day, Kai Tong, Aishwarya H. Balwani, Eva L. Dyer, Peter J. Yunker, William C. Ratcliff
bioRxiv 2021.08.03.454982; doi: https://doi.org/10.1101/2021.08.03.454982
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De novo evolution of macroscopic multicellularity
G. Ozan Bozdag, Seyed Alireza Zamani-Dahaj, Penelope C. Kahn, Thomas C. Day, Kai Tong, Aishwarya H. Balwani, Eva L. Dyer, Peter J. Yunker, William C. Ratcliff
bioRxiv 2021.08.03.454982; doi: https://doi.org/10.1101/2021.08.03.454982

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