title: Analysis of phenotypic evolution in Dictyostelia highlights developmental plasticity as a likely consequence of colonial multicellularity.
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.
authors.affiliation: College of Life Sciences, University of Dundee, Dundee, UK.
authors.forename: Maria
authors.initials: M
authors.lastname: Romeralo
authors.forename: Anna
authors.initials: A
authors.lastname: Skiba
authors.forename: Alejandro
authors.initials: A
authors.lastname: Gonzalez-Voyer
authors.forename: Christina
authors.initials: C
authors.lastname: Schilde
authors.forename: Hajara
authors.initials: H
authors.lastname: Lawal
authors.forename: Sylwia
authors.initials: S
authors.lastname: Kedziora
authors.forename: Jim C
authors.initials: JC
authors.lastname: Cavender
authors.forename: Gernot
authors.initials: G
authors.lastname: Glöckner
authors.forename: Hideko
authors.initials: H
authors.lastname: Urushihara
authors.forename: Pauline
authors.initials: P
authors.lastname: Schaap
mesh_terms: D005075:Biological Evolution; D002630:Chemotactic Factors / Q000502:physiology; D000242:Cyclic AMP / Q000031:analogs & derivatives / Q000378:metabolism / Q000494:pharmacology; D016837:Dictyosteliida / Q000166:cytology* / Q000187:drug effects / Q000502:physiology*; D020412:Multifactorial Inheritance; D010641:Phenotype; D018524:Phototropism; D010802:Phylogeny; D011506:Proteins / Q000235:genetics; D013873:Thionucleotides / Q000494:pharmacology
chemical_list: D002630:Chemotactic Factors; D011506:Proteins; D013873:Thionucleotides; C016957:adenosine-3',5'-cyclic phosphorothioate; D000242:Cyclic AMP
keywords: encystation; evolution of multicellularity; morphogenetic signalling; phototropism; phylogenomics; sporulation