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The Single-Celled Ancestors of Animals: A History of Hypotheses

Thibaut Brunet , Nicole King

Preprint posted on November 10, 2020 https://www.preprints.org/manuscript/202011.0302/v1

Tracing the history of animal origins

Selected by Hiral Shah, Dey Lab

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).

Figure1: The ancestor with many unicellular forms and facultative multicellularity (from Figure 8 in Brunet and King, 2020, provided under CC-BY 4.0)

See questions and author response below!

References:

  1. Fairclough, S. R., Dayel, M. J. & King, N. Multicellular development in a choanoflagellate. Curr. Biol. CB 20, R875-876 (2010).
  2. Sebé-Pedrós, A. et al. Regulated aggregative multicellularity in a close unicellular relative of metazoa. eLife 2, e01287 (2013).
  3. Dudin, O. et al. A unicellular relative of animals generates a layer of polarized cells by actomyosin-dependent cellularization. eLife 8, e49801 (2019).
  4. 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).
  5. Brunet, T. et al. Light-regulated collective contractility in a multicellular choanoflagellate. Science 366, 326–334 (2019).
  6. Schardinger, F. 1899. “Entwicklungskreis Einer Amoeba Lobosa (Gymnamoeba): Amoeba Gruberi. Sitzb Kaiserl.” Akad. Wiss. Wien Abt. 1: 713–734.
  7. 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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Author response

Thibaut Brunet shared

Multicellularity has evolved multiple times independently in the history of life on earth. Do the authors’ recent insights into the origins of animal multicellularity have implications for those studying other convergent processes? 

It is not entirely easy to answer this question, because diversity is the essence of biology, and the multicellularity of animals is unique in several ways. One unusual aspect is that animals have “complex multicellularity”, which is obligate and involves large size, complex cell type complement, and regulated morphogenesis (as defined by Andy Knoll – doi: 10.1146/annurev.earth.031208.100209). This has evolved only five times (in animals, fungi, land plants, red algae and brown algae), while simple multicellularity is much more common. Moreover, animals are the only complex multicellular groups that have a phagotrophic lifestyle. While this makes it challenging to directly generalize any principle from animals to other multicellular groups, comparisons are certainly important and may allow some general principles to emerge.

One aspect emphasized in our review is the possible phenotypic complexity of the single-celled ancestor of animals, and the importance of studying multiple outgroups. This has interesting parallels in the evolution of land plants, whose closest relatives were long debated, but have been shown this year to apparently be the Zygnematophyceae. Interestingly, the multicellular forms of this lineage are morphologically simpler than those of the immediately more distant outgroups – and their genome indicates that Zygnematophyceae are indeed probably secondarily simplified (see Donoghue & Paps, 2020 – doi: 10.1016/j.cub.2019.11.084). So if you want to fully understand the genomic and phenotypic evolution of land plants, you cannot restrict yourself to the study of their closest relatives, but you might have to take into account more distant taxa as well. The same might be true regarding the single-celled relatives of animals: the model choanoflagellates Salpingoeca rosetta and Monosiga brevicollis do have a complex cell biology but seem to have lost some genes – and maybe also some cellular features – since the last choanozoan common ancestor. Interestingly, other choanoflagellate species are now known to have a much more conservative genome, and it would be interesting to study those more in detail, along with other unicellular holozoans (see this study by Dan Richter et al: https://elifesciences.org/articles/34226). Both of these case studies can serve as reminders that evolution does not always go toward more complexity, and that secondary simplification is probably be just as prevalent. It also reinforces the familiar lesson that no extant taxon can be assumed to be identical to our last common ancestor with it, even though some groups certainly have accumulated fewer morphological and molecular changes than others.

 

Scientists rarely take the time to dig into the history of their own field, even though doing this can yield surprising insights and uncover treasure buried in yellowing papers. Could the authors comment on how this exercise might influence their own work going forward?

The initial motivation for this historical summary was curiosity, and it is hard to predict what influence it might exert on our research in the future. Reading (ancient or recent) papers is often a good way to find new research directions, and old papers can be especially valuable because they usually take a very different perspective than one’s own, sometimes on the very same problem – the past, as they say, is a foreign country. Examples include the mysterious protists Magosphaera planula and Proterospongia haeckelii, observed only once, which would certainly be highly informative if they could be re-isolated; indeed, we have already spent some time looking for P. haeckelii (unsuccessfully so far!) 

But other examples are systems or problems that are now neglected, but used to captivate people at one time or another – science is not immune to fashion, and studying history can help realize that. For example, Haeckel was fascinated by the amoeboid egg of sponges, because he so strongly believed in recapitulation that he thought those eggs must reflect the phenotype of animal ancestors. His description of sponge eggs as amoeboid has been confirmed and replicated several times by sponge morphologists – their existence is not in doubt – but it attracted little general attention and is not necessarily widely known today. Nevertheless, even in other animals than sponges, egg cells are very often highly contractile and display complex intracellular actin dynamics, either before or after fertilization. This cytoskeletal dynamics of egg cells has been the object of recent beautiful studies by cell biologists, notably by the labs of Peter Lenart (doi:10.1038/s41467-017-02520-1) and Carl-Philipp Heisenberg (doi:10.1016/j.cell.2019.04.030). With Haeckel in mind, one might wonder if these actin-mediated deformation in animal eggs could be interpreted as a vestigial amoeboid motility that now serves other functions (such as redistribution of cytoplasmic content – including for example yolk granules). In the case of our own research on amoeboid mobility in choanoflagellates, it means that if we consider data from animals to investigate potential shared mechanisms, we should maybe not restrict ourselves to crawling cells like neutrophils or dendritic cells, but that we should maybe also pay attention to studies of oocytes!

 

One main difference between M. planula and Ichthyosporeans outlined by the authors is the absence of free-living Ichthyosporean species. In the past decade, at least three species have been isolated as free living including two Sphaeroforma species and Chromosphaera perkinsiiDo you think this would strengthen your suggestion that maybe M. planula could be an Ichthyosporean species?

We absolutely agree. Another open question is whether the type of serial dichotomous division described in Magosphaera exists in Ichthyosporeans, alongside the simultaneous cellularization described in known species. We hope that future work will help shed light on this question.

 

How do you think the nature of the unicellular ancestor of animals would change if M. planula and/or P. haeckelli were successfully re-isolated and all the previous observations were true?

We think this would largely depend on their phylogenetic position. For example, if P. haeckelii turned out to be sister to animals (closer to us than to other choanoflagellates), it would support a pre-metazoan origin for spatial cell differentiation. On the other hand, if it turned out to be nested deep within the evolutionary tree of choanoflagellates, then the most parsimonious interpretation would be that it evolved spatial cell differentiation independently of metazoans – which would still make it a very interesting model system, but would have less influence on ancestral state reconstructions. An exciting aspect is that the phylogenetic position of these species was a very speculative, open question for Saville-Kent and Haeckel, but that we would have much better chances of determining it if we could get genomic data. In general, studying these species with a modern technical toolkit would allow us to answer many of the questions Haeckel and Saville-Kent asked, but could not answer at the time.  

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