DOI: 10.5061/dryad.7wm37pvzf
title: Conflict reducing innovations in development enable increased multicellular complexity

description: 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 few cells and cell-types, and others billions of cells and
 thousands of types. Here, we test if variation in multicellular complexity
 is explained by conflict-suppressing mechanisms, namely a single cell
 bottleneck at the start of development, and a strict separation of
 germline and somatic cells. Applying a phylogenetic comparative analysis
 to the life-cycles 138 lineages of plants, animals, fungi and algae, we
 show that an early segregation of the germline stem-cell lineage is key to
 the evolution of more cell types. In contrast, the presence of a strict
 single cell bottleneck was not related to either the number of cells or
 cell types but was associated with early germline segregation. Our results
 suggest that segregating the germline earlier in development enabled
 greater evolutionary innovation, possibly through conflict suppression or
 via greater developmental flexibility. 
description: # Conflict reducing innovations in development enable increased
 multicellular complexity 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.
 #### 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
 . 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.