Howe, J. Copenhagen University.

Cornwallis, C. K. Lund University.

Griffin, A. S. Oxford University.

Cite this dataset

Howe, Jack; Cornwallis, Charlie; Griffin, Ashleigh (2024). Conflict reducing innovations in development enable increased multicellular complexity [Dataset]. Dryad. https://doi.org/10.5061/dryad.7wm37pvzf

Abstract

Obligately multicellular organisms, where cells can only reproduce as part of the group, have evolved multiple times across the tree of life. Obligate multicellularity has only evolved when clonal groups form by cell division, rather than by cells aggregating, as clonality prevents internal conflict. Yet obligately multicellular organisms still vary greatly in ‘multicellular complexity’ (the number of cells and cell types): some comprise a few cells and cell types, while others have billions of cells and thousands of types. Here, we test whether variation in multicellular complexity is explained by two conflict-suppressing mechanisms, namely a single-cell bottleneck at the start of development, and a strict separation of germline and somatic cells. Examining the life cycles of 129 lineages of plants, animals, fungi and algae, we show using phylogenetic comparative analyses that an early segregation of the germline stem-cell lineage is key to the evolution of more cell types, driven by a strong correlation in the Metazoa. By contrast, the presence of a strict single-cell bottleneck was not related to either the number of cells or the number of cell types, but was associated with early germline segregation. Our results suggest that segregating the germline earlier in development enabled greater evolutionary innovation, although whether this is a consequence of conflict reduction or other non-conflict effects, such as developmental flexibility, is unclear.

Usage notes

This Dryad entry and its linked Zenodo deposit are a copy of the GitHub repo found at https://github.com/jackhowe-bio/complexity_project. The GitHub repo contains all data and code for all analyses in the manuscript.

The Data folder contains the data and associated references.

The RScripts folder contains all the scripts for running the analysis.

To run, edit line 2 of RScripts/RunAllAnalyses.R to reflect your working dir. Then cd to this directory, and run RScript RScripts/RunAllAnalyses.R. This will run all permutations of the analyses that are presented in the manuscript. It will create the Results folder, and all files and folders within it-- including the figures that are presented in the manuscript (although some small edits to legend position and labels were made using illustrator/inkscape).

The supplementary information is produced by using RMarkdown, by the file SupplementaryInfoUpdating.Rmd. It is reliant on the above scripts having been run.

The data (referred to as "germline_data_1.5.csv" in the github repo) were extracted from published literature. All references cited in the dataset can be found in the references tab (referred to as "ReferencesPlainText.docx" in the github repo).

Datasets included on Dryad:

1) The number of cells and cell types across multicellular species in relation to their life cycles.

Column headings for "germline_data_1.5.csv" sheet are:

• species: species name in the R Tree of Life Project.

• species_orginal_name: original species name.
• -Obligate_or_facultative: If species are obligately or facultatively multicellularity. Only obligate species were included in analyses.
• Simple_or_complex: simple defined in paper as "fewer than a dozen cells with no discernible cell types".
• Sterile_soma: somatic cells do not give rise to new individuals.
• Proportion_of_sterile cells: average proportion of cells that are sterile.
• cell_types: number of differentiated cell types.
• cell_number: average number of cells per multicellular individual.
• clonal: all cells genetically identical.
• Fisher_ref: Reference for taxa cited by Fisher et al 2013 Current Biology.
• Kingdom: taxonomic classification.
• phylum: taxonomic classification.
• class: taxonomic classification.
• order: taxonomic classification.

• taxon: taxonomic classification.

• SexualReproductionObserved_Species: does species reproduce sexually 1=yes, 0=no.

• AsexualGameticObserved_Species: does species produce asexual gametes 1=yes, 0=no.

• FissionOrBuddingObserved_Species: do new multicellular individuals of species form by fission or budding 1 = yes, 0=no.

• SexualReproductionObserved_Genus: does genus reproduce sexually 1=yes, 0=no.

• AsexualGameticObserved_Genus: does genus produce asexual gametes 1=yes, 0=no.

• FissionOrBuddingObserved_Gneus: do new multicellular individuals within genus form by fission or budding 1 = yes, 0=no.

• notes: any relevant notes about data.

• germline_timing: 3 = early germline segregation, 1 & 2 = late germline segregation, 0 = no germline.

• References: number of reference in "Reference" sheet used to extract data.

Note: NA = missing data. Where data were missing for species, genus level data was used.

Column headings for "References" sheet are:

• Number_in_table: number that corresponds to "germline_data_1.5.csv"" sheet.
• Reference: Literature used to extract data on species and genera.

Funding

J.H. was supported by the Carlsberg Foundation (CF20_0541), A.S.G. by the Volkswagen Foundation (94818) and the Natural Environment Research Council (NE/V011537/1), and C.K.C. by a Wallenberg Academy fellowship (2018.0138), the Crafoord Foundation (20210788) and the Swedish Research Council (2022-03503). This research was funded in whole, or in part, by the UKRI (NE/ V011537/1). For the purpose of open access, the A.S.G. has applied a CC BY public copyright licence to any author accepted manuscript version arising from this submission.