Dataset Information

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.

SUBMITTER: Herron MD

PROVIDER: S-EPMC2651347 | biostudies-literature | 2009 Mar

REPOSITORIES: biostudies-literature

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Publications

Triassic origin and early radiation of multicellular volvocine algae.

Herron Matthew D MD Hackett Jeremiah D JD Aylward Frank O FO Michod Richard E RE

Proceedings of the National Academy of Sciences of the United States of America 20090217 9

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 it ...[more]

PMID: 19223580

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Project description:Colonial Volvocine Algae (CVA) are of great significance for biological evolution study, but little is presently known about their biogeographic distribution. Meanwhile, with the impact of climate change and human activities, their effects on the distribution and structures of CVA communities also remain largely unknown. Herein, the biogeography of CVA was investigated in the Yangtze River basin, 172 sampling sites were set up within a catchment area of 1,800,000 km2, and the distribution and community composition of CVA were studied using single-molecule real-time sequencing and metabarcoding technology based on the full-length 18S sequence. In 76 sampling sites, CVA was discovered in two families, eight genera, and nine species. Eudorina and Colemanosphaera were the main dominant genus. Based on the result of the random forest model and Eta-squared value, the distribution of CVA was significantly influenced by water temperature, altitude, and TP. CVA could be suitably distributed at an average water temperature of 22°C, an average TP concentration of 0.06 mg/L, and an altitude lower than 3,920 m. To assess the effects of anthropogenic pollution on the structures and co-occurrence patterns of CVA communities, we used a stress index calculated by 10 environmental factors to divide the CVA community into low and high pollution group. Network analysis showed that greater pollution levels would have a negative impact on the co-occurrence patterns and diversity of the CVA community. Finally, to study the scientific distribution of CVA under current and future climate change scenarios, we analyzed the climate suitability regionalization of CVA with the maximum entropy model based on 19 climatic factors and four climate scenarios from 2021 to 2040 published by CMIP6. Our results reveal the suitable areas of CVA, and temperature is an important environmental factor affecting the distribution of CVA. With the change of climate in the future, the Three Gorges Reservoir Area, Chaohu Lake, and Taihu Lake are still highly suitable areas for CVA, but the habitat of CVA may be fragmented, and more thorough temporal surveys and sampling of the sediment or mud are needed to investigate the fragmentation of CVA.

Project description:The volvocine lineage, containing unicellular Chlamydomonas reinhardtii and differentiated multicellular Volvox carteri, is a powerful model for comparative studies aiming at understanding emergence of multicellularity. Tetrabaena socialis is the simplest multicellular volvocine alga and belongs to the family Tetrabaenaceae that is sister to more complex multicellular volvocine families, Goniaceae and Volvocaceae. Thus, T. socialis is a key species to elucidate the initial steps in the evolution of multicellularity. In the asexual life cycle of C. reinhardtii and multicellular volvocine species, reproductive cells form daughter cells/colonies by multiple fission. In embryogenesis of the multicellular species, daughter protoplasts are connected to one another by cytoplasmic bridges formed by incomplete cytokinesis during multiple fission. These bridges are important for arranging the daughter protoplasts in appropriate positions such that species-specific integrated multicellular individuals are shaped. Detailed comparative studies of cytokinesis between unicellular and simple multicellular volvocine species will help to elucidate the emergence of multicellularity from the unicellular ancestor. However, the cytokinesis-related genes between closely related unicellular and multicellular species have not been subjected to a comparative analysis.Here we focused on dynamin-related protein 1 (DRP1), which is known for its role in cytokinesis in land plants. Immunofluorescence microscopy using an antibody against T. socialis DRP1 revealed that volvocine DRP1 was localized to division planes during cytokinesis in unicellular C. reinhardtii and two simple multicellular volvocine species T. socialis and Gonium pectorale. DRP1 signals were mainly observed in the newly formed division planes of unicellular C. reinhardtii during multiple fission, whereas in multicellular T. socialis and G. pectorale, DRP1 signals were observed in all division planes during embryogenesis.These results indicate that the molecular mechanisms of cytokinesis may be different in unicellular and multicellular volvocine algae. The localization of DRP1 during multiple fission might have been modified in the common ancestor of multicellular volvocine algae. This modification may have been essential for the re-orientation of cells and shaping colonies during the emergence of multicellularity in this lineage.

Project description:BackgroundThe 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.ResultsWe 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.ConclusionsAltogether, 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.

Dataset Information

Triassic origin and early radiation of multicellular volvocine algae.

Publications

Triassic origin and early radiation of multicellular volvocine algae.

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