Exploring the ecological and evolutionary consequences of clonal and aggregative development during the transition to multicellularity
Pentz, Jennifer T
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Multicellular organisms form groups in one of two basic ways: cells can ‘stay together’ due to incomplete separation following cellular division (clonal development), or cells can ‘come together’ via aggregation (aggregative development). Multicellularity has evolved multiple times via both routes, but all ‘complex multicellularity’ (e.g., plants, animals, fungi) has only evolved in lineages that develop clonally. Evolutionary theory predicts that clonal development may be superior to aggregation because groups formed this way have little among-cell genetic conflict, thereby aligning the fitness interests of lower-level units (cells), increasing the potential for groups to undergo an ‘evolutionary transition in individuality’ (ETI). ETIs are characterized by a hierarchical shift in the level at which heritable variation in fitness is expressed (e.g., from cells to the multicellular group). In this dissertation, I compare clonal and aggregative development in a simple yeast (Saccharomyces cerevisiae) model system. First, I performed a selection experiment using wild-isolated aggregative yeast (termed flocs) with daily selection for rapid sedimentation in liquid medium. Clonally-developing yeast (termed ‘snowflake yeast’) arose and displaced flocs, and invading snowflake yeast showed higher fitness than their floc counterparts. Next, I engineered snowflake and floc yeast from a common unicellular ancestor, so these two strains only differ in their mode of cluster development. In monoculture, floc yeast were superior to snowflake yeast, growing faster and forming larger clusters that settling more rapidly. Yet, in direct competition, snowflake yeast exploit flocs, becoming disproportionately represented within fast-settling groups. Modeling suggests that ‘choosy’ flocs that exclude snowflake yeast would have the highest fitness, but such a strain would not be able to invade from rare. Finally, I performed a long-term evolution experiment to compare the dynamics of multicellular adaptation in floc and snowflake yeast by selecting for increasingly large cluster size, a multicellular trait. Our environment introduces two important life history traits that affect fitness, growth (cell level) and settling (cluster level), and evolved floc and snowflake yeast exhibited fitness gains in these two opposing traits, respectively. Furthermore, snowflake yeast were enriched with mutations that decrease fitness at the single-cell level, but may be beneficial at the cluster-level. Over evolutionary time, this could result in cells becoming interdependent parts of a new multicellular individual. Taken together, these results show that non-clonal cellular binding may be beneficial in environments favoring rapid multicellular group formation, but this paves the way for persistent evolutionary conflict. Conversely, simple clonal multicellular life cycles increase the efficacy of cluster-level adaptation relative to cell-level, which can potentiate an ETI and establish the emergent multicellular cluster as the new level of biological organization. These results highlight the critical role early multicellular life cycles play in driving – or constraining – this major evolutionary transition.