Triassic origin and early radiation of multicellular volvocine algae

Abstract

Evolutionary transitions in individuality (ETIs) underlie the watershed events in the history of life on Earth, including the origins of cells, eukaryotes, plants, animals, and fungi. Each of these events constitutes an increase in the level of complexity, as groups of individuals become individuals in their own right. Among the best-studied ETIs is the origin of multicellularity in the green alga Volvox, a model system for the evolution of multicellularity and cellular differentiation. Since its divergence from unicellular ancestors, Volvox has evolved into a highly integrated multicellular organism with cellular specialization, a complex developmental program, and a high degree of coordination among cells. Remarkably, all of these changes were previously thought to have occurred in the last 50-75 million years. Here we estimate divergence times using a multigene data set with multiple fossil calibrations and use these estimates to infer the times of developmental changes relevant to the evolution of multicellularity. Our results show that Volvox diverged from unicellular ancestors at least 200 million years ago. Two key innovations resulting from an early cycle of cooperation, conflict and conflict mediation led to a rapid integration and radiation of multicellular forms in this group. This is the only ETI for which a detailed timeline has been established, but multilevel selection theory predicts that similar changes must have occurred during other ETIs.

Fig. 1.

Chronogram showing estimated divergence times among photosynthetic eukaryotes. Blue bars are the central 95% of estimates from 300 Bayesian posterior trees. Red bars are the central 95% of dates inferred during fossil cross-validation. Bayesian posterior probabilities <0.95 are shown. References for the fossil calibrations are given in the text. The green circle indicates the most recent common ancestor of Paulschulzia pseudovolvox and Volvox carteri, the divergence used to calibrate the fine-scale analyses.

Fig. 2.

Chronogram showing estimated divergence times among volvocine algae. Colored boxes identify the 3 multicellular families; ingroup species not highlighted in this manner are unicellular (Paulschulzia pseudovolvox, the outgroup, represents a separate origin of multicellularity). Blue bars are the central 95% of estimates from 300 Bayesian posterior trees. Bayesian posterior probabilities <0.95 are shown. The green circle indicates the calibration estimated in the broad-scale analyses. Red letters indicate nodes referred to in the text. Character state changes are those supported by hypothesis tests in ref. . We have retained Kirk's (4) original numbering for these steps. *, steps 11 and 12 may have had 2 separate origins in the clade including V. africanus and V. carteri.