Phylotranscriptomics points to multiple independent origins of multicellularity and cellular differentiation in the volvocine algae

The volvocine algae, which include the single-celled
species Chlamydomonas reinhardtii and the colonial
species Volvox carteri, serve as a model in which to study the
evolution of multicellularity and cellular differentiation. Studies
reconstructing the history of this group have by and large relied on
datasets of one to a few genes for phylogenetic inference and ancestral
character state reconstruction. As a result, volvocine phylogenies lack
concordance depending on the number and/or type of genes (i.e.,
chloroplast vs nuclear) chosen for phylogenetic inference. While multiple
studies suggest that multicellularity evolved only once in the volvocine
algae, that each of its three colonial families is monophyletic, and that
there have been at least three independent origins of cellular
differentiation in the group, other studies call into question one or more
of these conclusions. An accurate assessment of the evolutionary history
of the volvocine algae requires inference of a more robust
phylogeny. We performed RNA sequencing (RNA-seq) on 55 strains
representing 47 volvocine algal species and obtained similar data from
curated databases on 13 additional strains. We then compiled a dataset
consisting of transcripts for 40 single-copy, protein-coding, nuclear
genes, and subjected the predicted amino acid sequences of these genes to
maximum likelihood, Bayesian inference, and coalescent-based analyses.
These analyses show that multicellularity independently evolved at least
twice in the volvocine algae and that the colonial family Goniaceae is not
monophyletic. Our data further indicate that cellular differentiation
arose independently at least four, and possibly as many as six times,
within the volvocine algae. Altogether, our results demonstrate
that multicellularity and cellular differentiation are evolutionarily
labile in the volvocine algae, affirming the importance of this group as a
model system for the study of major transitions in the history of life.