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Review
, 101 (1), 6-25

The Evolutionary-Developmental Origins of Multicellularity

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Review

The Evolutionary-Developmental Origins of Multicellularity

Karl J Niklas. Am J Bot.

Abstract

Multicellularity has evolved at least once in every major eukaryotic clade (in all ploidy levels) and numerous times among the prokaryotes. According to a standard multilevel selection (MLS) model, in each case, the evolution of multicellularity required the acquisition of cell-cell adhesion, communication, cooperation, and specialization attended by a compulsory alignment-of-fitness phase and an export-of-fitness phase to eliminate cell-cell conflict and to establish a reproductively integrated phenotype. These achievements are reviewed in terms of generalized evolutionary developmental motifs (or "modules") whose overall logic constructs were mobilized and executed differently in bacteria, plants, fungi, and animals. When mapped onto a matrix of theoretically possible body plan morphologies (i.e., a morphospace), these motifs and the MLS model identify a "unicellular ⇒ colonial ⇒ multicellular" transformation series of body plans that mirrors trends observed in the majority of algae (i.e., a polyphyletic collection of photoautotrophic eukaryotes) and in the land plants, fungi, and animals. However, an alternative, more direct route to multicellularity theoretically exists, which may account for some aspects of fungal and algal evolution, i.e., a "siphonous ⇒ multicellular" transformation series. This review of multicellularity attempts to show that natural selection typically acts on functional traits rather than on the mechanisms that generate them ("Many roads lead to Rome.") and that genome sequence homologies do not invariably translate into morphological homologies ("Rome isn't what it used to be.").

Keywords: Spitzenkörper; algae; animals; bacteria; body plans; coenocyte; cytokinesis; dynamic patterning modules; embryophytes; evolution; fungi; multilevel selection (MLS) theory; phragmoplast; siphonous.

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