In partial fulfillment of the requirements for the degree of

Doctor of Philosophy in Quantitative Biosciences

in the School of Biological Sciences

Rozenn M. Pineau

Will defend her dissertation
Evolution in real time: insights from micro- to macroscopic multicellular organisms

Monday, October 2, 2023

2:00pm Eastern

Engineered Biosystems Building, Children's Healthcare of Atlanta Seminar Room (EBB 1005)

Zoom link: https://gatech.zoom.us/j/92303092893

Advisor:
Dr. William C. Ratcliff, School of Biological Sciences, Georgia Institute of Technology

Committee members:

Dr. Peter J. Yunker, School of Physics, Georgia Institute of Technology

Dr. Jenny L. McGuire, School of Biological Sciences, Georgia Institute of Technology

Dr. Ozan G. Bozdag, School of Biological Sciences, Georgia Institute of Technology

Dr. Zach Gompert, Department of Biology, Utah State University

Abstract:

Multicellularity has evolved independently at least 50 times and fundamentally transformed life on Earth, yet basic questions remain about how this transition initially occurs and shapes ecological dynamics. Understanding this transition and its underlying mechanisms is essential to better understand the evolution of life on Earth.

The first part of this work examines the emergence of a common yet understudied multicellular organism morphology, cuboidal packing. Spherical fission yeast (Schizosaccharomyces pombe) mutants were experimentally evolved via daily settling selection favoring larger size. Within 20 days, multicellular clusters evolved cuboidal cellular packing, a topology found across the tree of life. These clusters displayed traits of multicellular individuals: reproduction via cluster fracture, heritability in size, and response to group selection. Our genetic analysis reveals mutations in the ACE2 gene underlying this transition to multicellularity. This is an example of a deep convergent evolution, as this gene has also been implicated in the transition to multicellularity in Saccharomyces cerevisiae, a yeast species that diverged from S. pombe 300 millions of years ago.

Next, we explore the ecological implications of the transition to multicellularity and show how the formation of groups itself is an opportunity for niche expansion and divergence. Using long-term experimental evolution of snowflake yeast (S. cerevisiae), we show that the fundamental trade-off between growth and survival facilitated the evolution of two distinct coexisting phenotypes: one Small phenotype specialized in growth, and one Large phenotype specialized in survival. Coexistence is maintained by negative frequency dependent selection, and sequencing reveals that the dominant lineages present after 715 daily transfers have coexisted throughout the duration of the experiment. This work demonstrates how a simple and yet fundamental trade-off between growth and survival can immediately drive adaptive diversification and maintain increased ecological diversity. 

Finally, the last part of this dissertation sheds light on mutation dynamics in complex and ancient multicellular organisms. We explore the evolutionary history of an ancient and still-living clonal forest, the Pando aspen clone (Populus tremuloides). Harnessing the genetic signal generated by the accumulation of somatic mutations in the different tissues of the Pando clone, we detect spatial genetic structure, and estimate Pando's minimum age around 2,000 years.

Together, this thesis uses experimental evolution in unicellular microbes and natural experiments in clonal macrobes, contributing fundamental knowledge to our understanding of multicellular evolution, from the initial emergence of multicellular groups to the formation of complex, ancient organisms.