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

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.

Single-cell adaptations shape evolutionary transitions to multicellularity in green algae

“…Therefore it is unclear whether multicellularity is an adaptive response or is a correlated by-product of changes in other traits responding to environmental stimuli, such as cell size or extracellular excretions 36 . Second, the effects of predation and nutrients have largely been examined in isolation and independently from other environmental factors that may modify the costs and benefits of multicellularity [11][12][13][14][15]31 . For example, in aquatic environments, nutrient levels and the success of predators in capturing unicellular versus multicellular prey may be modified by water turbulence 37 .…”

“…Here we use phylogenetic comparative analyses to examine the ecological conditions that explain multicellularity in green algae distributed across Swedish lakes using a combination of experiments and long-term lake-monitoring data. Green algae of the order Chlamydomonadales are an important model system for studying multicellularity 3,12,40,41 . Predation and nutrient levels have repeatedly been shown to induce the formation of multicellular groups in unicellular species, and there are multiple origins of obligately multicellular species, some of which, such as Volvox and Pleodorina, have differentiated cell types 12,41,42 .…”

“…Green algae of the order Chlamydomonadales are an important model system for studying multicellularity 3,12,40,41 . Predation and nutrient levels have repeatedly been shown to induce the formation of multicellular groups in unicellular species, and there are multiple origins of obligately multicellular species, some of which, such as Volvox and Pleodorina, have differentiated cell types 12,41,42 . We examined 35 unicellular strains (genetically distinct 18S lineages from 19 species that span the Chlamydomonadales phylogeny), 33 of which were collected from ten different lakes and two that are commonly used reference strains (Fig.…”

“…1 and Supplementary Table 1). Each strain was exposed to varying levels of predation (Brachionus calyciflorus previously shown to induce multicellularity 12,31 ), nutrients (high versus low nitrate levels) and water turbulence (still versus turbulent). The different environmental variables were manipulated in a factorial design, and responses were monitored over 14 days (~14-28 generations (that is, mitotic cell divisions) 43 , Supplementary Tables 2 and 3).…”

“…Unicellular species that form multicellular groups in response to environmental stimuli ('facultative multicellularity') can provide insight into the ecological benefits of multicellularity [9][10][11][12][13][14][15][16] . Studies on diverse facultatively multicellular taxa have led to the predominant view that predation and nutrient availability are primary factors driving the evolution of multicellularity 1,3,17,18 .…”