Pluripotency and the origin of animal multicellularity

Abstract

The most widely held, but rarely tested, hypothesis for the origin of animals is that they evolved from a unicellular ancestor with an apical cilium surrounded by a microvillar collar that structurally resembled modern sponge choanocytes and choanoflagellates 1-4. Here we test this traditional view of animal origins by comparing the transcriptomes, fates and behaviours of the three primary sponge cell types-choanocytes, pluripotent mesenchymal archeocytes and epithelial pinacocytes-with choanoflagellates and other unicellular holozoans. Unexpectedly, we find the transcriptome of sponge choanocytes is the least similar to the transcriptomes of choanoflagellates and is significantly enriched in genes unique to either animals or sponges alone. In contrast, pluripotent archeocytes up-regulate genes controlling cell proliferation and gene expression, as in other metazoan stem cells and in the proliferating stages of two unicellular holozoans, including a colonial choanoflagellate. Choanocytes in the sponge Amphimedon queenslandica exist in a transient metastable state and readily transdifferentiate into archeocytes, which can differentiate into a range of other cell types. These sponge cell type conversions are similar to the temporal cell state changes that occur in unicellular holozoans 5. Together, these analyses offer no support for the homology of sponge choanocytes and choanoflagellates, nor for the view that the first multicellular animals were simple balls of cells with limited capacity to differentiate. Instead, our results are consistent with the first animal cell being able to transition between multiple states in a manner similar to modern transdifferentiating and stem cells. References 1 Cavalier-Smith, T. Origin of animal multicellularity: precursors, causes, consequences-the choanoflagellate/sponge transition, neurogenesis and the Cambrian explosion.

The significance of sponges for comparative studies of developmental evolution

“…Testing the hypothesis of homology between choanocyte/choanoflagellate feeding structures is no less fraught with difficulty when using gene expression data. A recent study (Sogabe et al, ) compares the expression profile of three sponge cell types to choanoflagellates and finds no particular similarity with choanocytes. Rather, 43% of the upregulated genes in choanocytes are restricted to the sponge lineage (46% of all genes in the genome are sponge‐exclusive).…”

A flagellate-to-amoeboid switch in the closest living relatives of animals

“…4o,p). This switch would have remained reversible at first (as it still is in sponges 34 ; Fig. 4o) but later become irreversible with the evolution of terminal cell differentiation (Fig.…”

“…The close evolutionary relationship between animals and choanoflagellates 20 , coupled with the similarity of morula stage animal embryos to spherical colonies of choanoflagellates 30 lent apparent support to Metschnikoff’s hypothesis 25 and led us and others to infer that the amoeboid cell types of animals had evolved from ancestral flagellate cells 25,31–33 after the establishment of multicellularity. However, modern choanoflagellates doubtless differ in some respects from their last common ancestor with animals 34 and some close outgroups to choanoflagellates and animals produce amoeboid cells 3,8,20,35,36 (some of which have recently been shown to alternate with a flagellate form 37–39 ), raising the possibility that the cellular machinery for cell crawling and flagellar swimming both predate the divergence of the choanoflagellate and animal lineages 16 . Intriguingly, rare and transient episodes of cell deformation have been reported to precede cell division in certain types of choanoflagellates 22 .…”

“…o , In sponges, the zygote can give rise to flagellated choanocytes and amoeboid archeocytes. Choanocytes and archeocytes can reversibly interconvert, but this process takes several hours and likely requires transcriptional regulation 34 . p , In vertebrates, multicellular development from the zygote results in terminal differentiation of ciliated epithelial cells, mesenchymal cells and amoeboid leukocytes, but injury can trigger differentiation of epithelial cells into crawling mesenchymal cells (by epithelial-to-mesenchymal transition, or EMT) that are respond to confinement switching into a stable bleb form that is capable of amoeboid migration 11 .…”

“…Finally, future comparative work will benefit from deeper insights into the mechanisms of cell crawling in choanoflagellates and animals 8 . Intriguingly, the amoeboid cell types of sponges (archeocytes) express more genes shared with choanoflagellates than other sponge cell types do 34 (including choanocytes), which might include genes involved in crawling motility 3 . Functional characterization 82 of those genes 8 in multiple phylogenetically relevant species as well as large-scale efforts to map animal cell type diversity within a phylogenetic framework 83,84 will help reveal how cell types have evolved and diversified during animal evolution.…”