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

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 perkinsii. Do 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.