Clonal-aggregative multicellularity tuned by salinity in a choanoflagellate.

Abstract

Multicellularity evolved independently multiple times in eukaryotes^1-4. Two distinct mechanisms underpin multicellularity⁵: clonality (serial cell division without sister-cell separation) and aggregation (whereby independent cells assemble into a multicellular entity). Clonal and aggregative multicellularity are traditionally considered to be mutually exclusive^1,6-8, with rare exceptions⁹, and evolutionary hypotheses have addressed why multicellularity might diverge towards one or the other extreme^3,4. Both animals and their sister group, the choanoflagellates, are currently known to acquire multicellularity only clonally^4,10,11. Here we show that the choanoflagellate Choanoeca flexa¹² forms motile and contractile cell monolayers (sheets) through multiple mechanisms-C. flexa sheets can form purely clonally, purely aggregatively or through a combination of both processes. We characterize the life history of C. flexa in its natural environment-ephemeral splash pools on the island of Curaçao-and show that C. flexa undergoes reversible transitions between unicellularity and multicellularity during evaporation-refilling cycles. Different splash pools house genetically distinct strains of C. flexa and kin recognition constrains aggregation between them. We show that clonal-aggregative multicellularity is a versatile strategy for the robust establishment of multicellularity in this variable and fast-fluctuating environment. Our findings challenge former generalizations about choanoflagellates and expand the option space of choanozoan multicellularity.