Abstract
Colony formation was the first step towards evolution of multicellularity in many macroscopic organisms. Dictyostelid social amoebas have used this strategy for over 600 Myr to form fruiting structures of increasing complexity. To understand in which order multicellular complexity evolved, we measured 24 phenotypic characters over 99 dictyostelid species. Using phylogenetic comparative methods, we show that the last common ancestor (LCA) of Dictyostelia probably erected small fruiting structures directly from aggregates. It secreted cAMP to coordinate fruiting body morphogenesis, and another compound to mediate aggregation. This phenotype persisted up to the LCAs of three of the four major groups of Dictyostelia. The group 4 LCA co-opted cAMP for aggregation and evolved much larger fruiting structures. However, it lost encystation, the survival strategy of solitary amoebas that is retained by many species in groups 1–3. Large structures, phototropism and a migrating intermediate ‘slug’ stage coevolved as evolutionary novelties within most groups. Overall, dictyostelids show considerable plasticity in the size and shape of multicellular structures, both within and between species. This probably reflects constraints placed by colonial life on developmental control mechanisms, which, depending on local cell density, need to direct from 10 to a million cells into forming a functional fructification.
Highlights
A central problem in biology is to understand how complex multicellular life forms evolved from unicellular ancestors
Higher plants and animals have converted to zygotic multicellularity, colonial or aggregative multicellularity still occurs in many eukaryote kingdoms, such as Chromalveolata [2], Excavata [3], Amoebozoa [4,5] and Opisthokonta [6]
We have measured 21 traits that were partially covered by the original diagnoses and we investigated deeper traits, such as the alternative survival strategy of encystation, the ability to form motile ‘slugs’ and the identity of the signals that coordinate cell movement during aggregation and morphogenesis
Summary
A central problem in biology is to understand how complex multicellular life forms evolved from unicellular ancestors. Dictyostelid social amoebas offer unique opportunities to resolve this problem They are a genetically diverse group [7], which contains species that form structures of less than 100 cells and one or two cell types to species that can organize up to a million amoebas in a fruiting body consisting of five different cell types [4,8,9,10]. The SSU rDNA_32 protein phylogeny (see the electronic supplementary material, figure S5) was combined with the matrices of continuous or coded categorical characters (sheets 2 and 3 of ‘Trait_Analysis’). All traits showed high lambda values (range 0.65– 0.94), indicating that this model provides an adequate fit to the data (see the electronic supplementary material, table S1). To correct for wrongly rejected null hypotheses in multiple comparisons, the threshold p-value for rejecting the null hypothesis (no correlation between datasets) was adjusted by a false discovery rate-based method [24]
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