Abstract
How animals evolved from a single-celled ancestor, transitioning from a unicellular lifestyle to a coordinated multicellular entity, remains a fascinating question. Key events in this transition involved the emergence of processes related to cell adhesion, cell-cell communication and gene regulation. To understand how these capacities evolved, we need to reconstruct the features of both the last common multicellular ancestor of animals and the last unicellular ancestor of animals. In this review, we summarize recent advances in the characterization of these ancestors, inferred by comparative genomic analyses between the earliest branching animals and those radiating later, and between animals and their closest unicellular relatives. We also provide an updated hypothesis regarding the transition to animal multicellularity, which was likely gradual and involved the use of gene regulatory mechanisms in the emergence of early developmental and morphogenetic plans. Finally, we discuss some new avenues of research that will complement these studies in the coming years.
Highlights
All extant animals living today diversified from a common multicellular ancestor, known as the last common ancestor (LCA) of animals or the animal LCA
We provide an updated reconstruction of these two evolutionary stages that are key to better understanding the transition to animal multicellularity: 1) the last unicellular ancestor of animals and 2) the animal LCA
We propose an updated hypothesis to explain the transition to animal multicellularity, stressing that animal foundations were laid before the origin of animals and that the gradual complexification of genetic regulatory mechanisms was key to the progressive acquisition of animal axial cell patterning and cell-type identity
Summary
Animals (Metazoa) are among the major groups of complex multicellular organisms. They rely on a wide variety of differentiated cell types that are spatially organized within physiological systems. Recent data from a broad representation of animal species, especially from non-bilaterian animals (sponges, ctenophores, placozoans and cnidarians), and from unicellular species related to animals, have enabled us to better answer these questions Their genome content, gene regulatory capabilities and biological features can be compared to reconstruct the cellular foundations of animal evolution and infer the minimal genomic complexity of both the last unicellular ancestor of animals and the animal LCA. We summarize current knowledge on the genetic toolkit, cell-type diversity and ecological context of these ancestors, inferred by comparative genomic analyses between animals with their closest unicellular relatives and between the earliest branching animals and those radiating later On this basis, we propose an updated hypothesis to explain the transition to animal multicellularity, stressing that animal foundations were laid before the origin of animals and that the gradual complexification of genetic regulatory mechanisms was key to the progressive acquisition of animal axial cell patterning and cell-type identity. We discuss some of the research areas that we predict will be key to studying animal origins in the coming years
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