The Evolutionary Ecology of Multicellularity: The Volvocine Green Algae as a Case Study

Abstract

Abstract The volvocine green algae in the order Volvocales are an ideal modelsystem for studying the unicellular-multicellular transition since they comprise an assemblage of lineages featuring varying degrees of complexity in terms of colony size, colony structure, and cellular specialization. Here, we have investigated the size-related advantages that might have caused single-celled volvocine algae to start living in groups, and the possible reasons for the evolution of cellular differentiation as group size increased, which created multicellular volvocine algae with germ-soma separation. Primordial cell clusters might have benefited from decreased predation, increased nutrient uptake, nutrient storage, and enhanced motility capabilities. We have tested these hypotheses by analyzing previous data on motility and growth rates in Volvocales. We have also compared the growth rates of the unicellular Chlamydomonas reinhardtii and Gonium pectorale, a 1–16 celled volvocine alga, at different nutrient concentrations, and measured predation rates on these species using the phagotrophic euglenoid Peranema trichophorum. Our analyses support the hypothesis that predation was an important selective pressure for the origin of multicellularity, but found no evidence that increased motility and nutrient uptake were advantages for the first cell groups. The extra-cellular matrix necessary for cell clustering might have been later co-opted for nutrient storage. With regards to cellular differentiation, we review a model inspired by the Volvocales that explains the dynamics of the transition to germ-soma differentiation as size increases. We found that flagellar motility constraints and opportunities were important driving forces for germ-soma separation in this group. We argue that germ-soma separation in Volvocales evolved to counteract the increasing costs of larger multicellular colonies.