Fossil-calibrated inference of divergence times among the Volvocine algae enables reconstruction of the steps that led to differentiated multicellularity

Throughout its nearly four-billion-year history, life has undergone
evolutionary transitions in which simpler subunits have become integrated
to form a more complex whole. Many of these transitions opened the door to
innovations that resulted in increased biodiversity and/or organismal
efficiency. The evolution of multicellularity from unicellular forms
represents one such transition, one that paved the way for cellular
differentiation, including differentiation of male and female gametes. A
useful model for studying the evolution of multicellularity and cellular
differentiation is the volvocine algae, a clade of freshwater green algae
whose members range from unicellular to colonial, from undifferentiated to
completely differentiated, and whose gamete types can be isogamous,
anisogamous, or oogamous. To better understand how multicellularity,
differentiation, and gametes evolved in this group, we used comparative
genomics and fossil data to establish a geologically calibrated roadmap of
when these innovations occurred. Our results, presented as ancestral-state
reconstructions, show that multicellularity arose independently twice in
this clade. Our chronograms indicate multicellularity evolved during the
Carboniferous-Triassic periods in Goniaceae + Volvocaceae, and possibly as
early as the Cretaceous in Tetrabaenaceae. Using divergence time estimates
we inferred when, and in what order, specific developmental changes
occurred that led to differentiated multicellularity and oogamy. We find
that in the volvocine algae the temporal sequence of developmental changes
leading to differentiated multicellularity is much as proposed by David
Kirk, and that multicellularity is correlated with the acquisition of
anisogamy and oogamy. Lastly, morphological, molecular, and divergence
time data suggest the possibility of cryptic species in Tetrabaenaceae.