Neoproterozoic origin and multiple transitions to macroscopic growth in green seaweeds

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Abstract The Neoproterozoic Era records the transition from a largely bacterial to a predominantly eukaryotic phototrophic world, creating the foundation for the complex benthic ecosystems that have sustained Metazoa from the Ediacaran Period onward. This study focusses on the evolutionary origins of green seaweeds, which play an important ecological role in the benthos of modern sunlit oceans and likely played a crucial part in the evolution of early animals by structuring benthic habitats and providing novel niches. By applying a phylogenomic approach, we resolve deep relationships of the core Chlorophyta (Ulvophyceae or green seaweeds, and freshwater or terrestrial Chlorophyceae and Trebouxiophyceae) and unveil a rapid radiation of Chlorophyceae and the principal lineages of the Ulvophyceae late in the Neoproterozoic Era. Our time-calibrated tree points to an origin and early diversification of green seaweeds in the late Tonian and Cryogenian periods, an interval marked by two global glaciations, with strong consequent changes in the amount of available marine benthic habitat. We hypothesize that the unicellular and simple multicellular ancestors of green seaweeds survived these extreme climate events in isolated refugia, and diversified following recolonization of benthic environments that became increasingly available as sea ice retreated. An increased supply of nutrients and biotic interactions such as grazing pressure has likely triggered the independent evolution of macroscopic growth via different strategies, including both true multicellularity, and multiple types of giant celled forms. Significance Statement Green seaweeds are important primary producers along coastlines worldwide, and likely played a key role in the evolution of animals. To understand their origin and diversification, we resolve key relationships among extant green algae using a phylotranscriptomic approach. We calibrate our tree using available fossil data, to reconstruct important evolutionary events such as transitions to benthic environments, and evolution of macroscopic growth. We estimate green seaweeds to have originated in the late Tonian/Cryogenian Period, followed by a marked Ordovician diversification of macroscopic forms. This ancient proliferation of green seaweeds likely modified shallow marine ecosystems, which set off an evolutionary arms race between ever larger seaweeds and grazers.

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