The Single-Celled Ancestors of Animals: A History of Hypotheses
Preprint posted on November 10, 2020 https://www.preprints.org/manuscript/202011.0302/v1
Categories: cell biology, evolutionary biology
Hiral Shah, Gautam Dey and Omaya Dudin
Context
All living animals evolved from the same unicellular ancestor. Understanding how this transition to multicellularity happened is a crucial part of our attempt to retrace our own origins. For several centuries now, scientists have been tackling this question from morphological, developmental and genetic perspectives. In their preprint, Thibaut Brunet and Nicole King paint a beautiful tribute to the pioneering evolutionary cell biologists that addressed the origins of animal multicellularity from the 16th to the 20th century. Their quest began with the realisation that all living organisms are made of cells and that they share a common ancestor. These two present-day facts took centuries to be widely accepted, however, and it was only at the end of the 19th century that the three most studied groups of unicellular organisms at the time, namely flagellates, ciliates and amoebae, were first considered as potential candidates for the ancestors of all animals.
Key Findings
Through a meticulous chronological description of the observations of Haeckel, Metchnikoff and William Saville-Kent, to cite just a few, the authors review the rise and fall of both the amoebae and ciliate theories about the nature of the common unicellular ancestor of all animals. Haeckel’s hypothesis for an amoeboid ancestor was inspired by the morphological similarities between amoeboid cells and animal egg cells. His arguments relied on his own theory of recapitulation (which has been debunked numerous times since) as well as his characterization of Magosphaera planula, an enigmatic organism considered to be the missing link between protists and animals. Saville-Kent, on the other hand, strongly advocated for a model of independent origins for different animal lineages: that sponges had evolved from choanoflagellates (first suggested by Metchnikoff) and all other animals originated from ciliates. This theory was displaced by the increase in genomic, phylogenetic and cell biological datasets obtained from phylogenetically relevant non-model species. These studies state unequivocally that animals represent a monophyletic group with choanoflagellates as the closest living relative.
The preprint dives deep into the lives of the scientists behind these hypotheses, providing a moving account of their time, their observations, their supporters and their rivalries. The strongest rivalry was between Haeckel and Saville-Kent about the phylogenetic position of sponges. Both of them went on to describe a mysterious unicellular organism, namely Magosphaera planula and Proterospongia haeckelli, that strengthened their respective theories. Both organisms, detailed through their sketches, represented unicellular protists with exciting multicellular life-forms. Although no one has ever re-isolated or seen Magosphaera or Proterospongia since, many similarities have been identified with unicellular holozoan lineages, which leaves us with some hope of their real presence.
Despite the now-established fact that choanoflagellates and animals share a common choanozoan ancestor, the authors go ahead and propose that this ancestor could have possessed a more complex life-cycle than that of choanoflagellates. This idea emanates from the developmental complexity observed in Filastereans and Ichthyosporeans – two protist lineages closely related to choanoflagellates and animals. If Choanoflagellates such as Salpinogoeca rosetta can undergo serial cell divisions to form rosette-like clonal colonies, amoeboid Filasterean Capsaspora owczarzaki cells can join together to form multicellular aggregates 1,2. Ichthyosporeans, which represent the closest analogy to Haeckel’s Magosphaera, form multinucleated coenocytes that undergo cytokinesis at a constant volume through a cellularization process recently described in Sphaeroforma arctica 3. Further, protists differentiate into other unicellular or multicellular forms in response to environmental cues. S. rosetta cells under confinement can retract the flagellum and switch to a contractile amoeba 4. Choanoeca flexa form multicellular sheets which undergo inversion, contracting and relaxing alternating between better swimmers and feeders 5. Shape-shifting among protists was observed by Schardiner and Zahkvatkin way back in the early 1900s while working with Naegleria, an amoeba that can transform into flagellate forms 6,7. Zahkvatkin’s proposal of an amoeboflagellate ancestor opened up the possibility of a flexible ancestor and provided the first link between protist life-cycles and animal origins. The phenotypic plasticity across many unicellular holozoans suggests that these traits emerged way before the emergence of the first metazoans. The emergence of cell biological and genomic analysis across a wide range of unicellular holozoans over the last decade and the revival of Zahkvatkin’s work paved the way for a more complex ancestor with extensive flexibility in transitioning from one cell type to another. While some are still in favour of a simpler or minimalistic ancestor with less morphological plasticity, others argue that the different cellular forms may not be restricted to those predicted for the maximalistic ancestor (figure 1).

See questions and author response below!
References:
- Fairclough, S. R., Dayel, M. J. & King, N. Multicellular development in a choanoflagellate. Curr. Biol. CB 20, R875-876 (2010).
- Sebé-Pedrós, A. et al. Regulated aggregative multicellularity in a close unicellular relative of metazoa. eLife 2, e01287 (2013).
- Dudin, O. et al. A unicellular relative of animals generates a layer of polarized cells by actomyosin-dependent cellularization. eLife 8, e49801 (2019).
- Brunet, T., Albert, M., Roman, W., Spitzer, D. C. & King, N. A flagellate-to-amoeboid switch in the closest living relatives of animals. http://biorxiv.org/lookup/doi/10.1101/2020.06.26.171736 (2020).
- Brunet, T. et al. Light-regulated collective contractility in a multicellular choanoflagellate. Science 366, 326–334 (2019).
- Schardinger, F. 1899. “Entwicklungskreis Einer Amoeba Lobosa (Gymnamoeba): Amoeba Gruberi. Sitzb Kaiserl.” Akad. Wiss. Wien Abt. 1: 713–734.
- Sachwatkin, A. A. 1956. Vergleichende Embryologie Der Niederen Wirbellosen: Ursprung Und Gestaltungswege Der Individuellen Entwicklung Der Vielzeller. Berlin: VEB Deutscher Verlag der Wissenschaften.
Posted on: 5th January 2021
doi: https://doi.org/10.1242/prelights.26776
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