De novoevolution of macroscopic multicellularity

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.

Varied solutions to multicellularity: The biophysical and evolutionary consequences of diverse intercellular bonds

“… 16 Cellular elongation resulted in a reduction of the packing fraction in these groups and, therefore, reduced cell crowding and mitigated stress accumulation. When daily selection for larger group size was extended to 600 days (3000 generations), the cell shape mutations became a dominant feature of the organisms, leading to highly elongated cells 25,45 that persisted even under diverse growth conditions. Changing cell-packing fraction can, therefore, be a highly effective strategy for controlling bond fracture rate, in some cases outperforming the strategy of simply strengthening intercellular bonds.…”

“…Importantly, this emergent heritability can be maintained for long periods of directional selection. In the longest-running evolution experiment of nascent multicellularity, Bozdag et al 25 found that snowflake yeast clusters subject to 600 rounds of selection for larger size evolved to be ∼20 000 times larger than their ancestor, with gradual changes in cell-level traits (mainly cell length) underlying dramatically increased multicellular size and biophysical toughness.…”

Evolutionary consequences of nascent multicellular life cycles

“…Our selection regime involved 24h of batch culture followed by daily selection for rapid sedimentation in liquid media [36]. This selective scheme has previously been shown to lead to sustained multicellular adaption [36,37,41,42] increasing the cluster size of snowflake yeast by up to 20,000-fold over 600 consecutive rounds of selection [42]. We have previously quantified the effect of settling selection on snowflake yeast by using a variety of tools (i.e., microscopy and flow cytometry [36,37,41,42]) that cannot be used for floc, because floc aggregates form dynamically as the clusters are settling.…”

Experimental evolution is not just for model organisms

“…Experimental evolution has also been used to investigate a particular major evolutionary innovation: the origin of multicellularity. An ongoing long-term experiment in yeast is being used to examine how groups of cells form and adapt as multicellular individuals [ 4 , 5 ], and experimental evolution has been used to show how cooperative metabolism [ 6 ] and predation escape [ 7 , 8 ] can drive the evolution of simple multicellularity. These experiments have helped to shape the way we think about this transition, showing that a process once thought to be rare and highly constrained may in fact be relatively easy.…”

“…arctica spends most of its life cycle as a unicellular organism, although it has a transient syncytial and multicellular phase like many microbes. By applying selection for rapid sedimentation through liquid media, a process that efficiently selects on organism size and has previously been used to drive the evolution of multicellularity in Saccharomyces cerevisiae [ 4 , 5 ], they are able to evolve this primarily unicellular relative of animals to form large, clonal, consistently multicellular groups within a matter of weeks ( Fig 1 ).…”