Somatic differentiation evolves rapidly and repeatedly through the modification of developmental plasticity

Plasticity has been proposed to facilitate the evolution of novelty, but it's unclear if it can drive a transition to a novel kind of individual. We report the experimental evolution of obligate somatic differentiation in Eudorina, a predominantly undifferentiated species that develops plastic somatic cells in response to cold stress. Eudorina is a species of volvocine algae, a clade in which cellular differentiation has evolved repeatedly. We exposed Eudorina from 2 lab lines and 46 course-based undergraduate research experience lines to repeated cold shock. Somatic differentiation evolved rapidly, with 21 of 48 lines (44%) exhibiting a larger proportion of differentiated colonies in baseline conditions. We also identified a lineage with obligate somatic differentiation; this is the first published example of the experimental evolution of obligate somatic differentiation. 11 lines, including the obligately differentiated one, also exhibited changes in the proportion of somatic cells per differentiated colony. The proportion of somatic cells in these lines converged with that of Pleodorina, a polyphyletic soma-differentiated volvocine algae genus. Genome sequencing revealed that 93% of genes mutated in the obligately differentiated line and not in the control had at least one homolog with soma-specific expression in obligately differentiated Volvox carteri or Astrephomene gubernaculifera and/or cold-induced expression in unicellular Chlamydomonas reinhardtii. Moreover, 72% of genes mutated in the obligately differentiated line and not in the control had homologs with both soma-specific expression and cold-induced expression. These genes all have regulatory mutations and lie at the intersection of cold shock and somatic differentiation regulatory modules. Our results provide the first empirical demonstration that the modification of plastic responses to the environment can drive the evolution of somatic differentiation, a key step in the evolution of a new kind of evolutionary individual.