  Organisms have increased in complexity through a series of major evolutionary
transitions, in which formerly autonomous entities become parts of a novel
higher-level entity. One intriguing feature of the higher-level entity after
some major transitions is a division of reproductive labor among its
lower-level units. Although it can have clear benefits once established, it is
unknown how such reproductive division of labor originates. We consider a
recent evolution experiment on the yeast Saccharomyces cerevisiae as a unique
platform to address the issue of reproductive differentiation during an
evolutionary transition in individuality. In the experiment, independent yeast
lineages evolved a multicellular "snowflake-like'' cluster form in response to
gravity selection. Shortly after the evolution of clusters, the yeast evolved
higher rates of cell death. While cell death enables clusters to split apart
and form new groups, it also reduces their performance in the face of gravity
selection. To understand the selective value of increased cell death, we create
a mathematical model of the cellular arrangement within snowflake yeast
clusters. The model reveals that the mechanism of cell death and the geometry
of the snowflake interact in complex, evolutionarily important ways. We find
that the organization of snowflake yeast imposes powerful limitations on the
available space for new cell growth. By dying more frequently, cells in
clusters avoid encountering space limitations, and, paradoxically, reach higher
numbers. In addition, selection for particular group sizes can explain the
increased rate of apoptosis both in terms of total cell number and total
numbers of collectives. Thus, by considering the geometry of a primitive
multicellular organism we can gain insight into the initial emergence of
reproductive division of labor during an evolutionary transition in
individuality.
