The Cheshire cat entered Adventure of Alice in a Magic Land famous for his disappearing actions: parts of his body vanished one after another until there was nothing left but his smooth smile. Scientists are trying to track the evolution of animals facing something that is equally curious. One might assume that farther into evolution, the properties of animals that have just evolved will disappear to a sort of 'minimal animal' still there. However, more and more data shows that these minimal animals may not be animals at all. Instead, sophisticated cellular processes that were once considered exclusive to animals were found in several unicellular eukaryotes: smiles without cats (multicellular)!
So how do scientists reconstruct the profound history of multicellularity? Notes for the oldest multicellular organisms studied directly are plants that grow from 30,000-year-old seeds stored in ice sheets (Yashina et al., 2012). However, multicellular life is much older than this. Fossils of multicellular red algae were 1.6 billion years ago (Bengtson et al., 2017), and fossils from multicellular fungi originated about one billion years ago (Loron et al., 2019).
The oldest animal fossils that are believed to be certain are around half a billion years (Bobrovskiy et al., 2018). Multicellularity arises independently in plants, fungi and animals (Brunet and King, 2017). Scientists are attracted to the unicellular ancestors of this group because they want to know whether every transition to multicellularity is driven by the same evolutionary forces. Unfortunately, fossils reveal little about the cell biology of these ancient organisms.
Charles Darwin is well aware of this challenge. To reconstruct the evolutionary history of an organism, he wrote About the Origin of Species"We must look exclusively at our ancestors; but this is almost never possible and we are in each case forced to see … collateral descendants from the same original parent form. "That is, one must hope that the characteristics of living organisms reveal the nature of their extinct ancestors.
Researchers now know that Darwin's idea of "living fossils" is too simple. There is no organism that is completely identical with its ancestors: genetic mutations constantly accumulate, driven by conflict, competition, and random chance. However, one can hope to reconstruct ancestors using patches of various ancestral traits that are preserved in various survivors.
The central theme of the emerging field of evolutionary cell biology is the study of organisms that provide as much information as possible about the past. One way to do this is to develop new model organisms based on their position in the tree of life. When animal evolution is traced back, ancestral unicellular species at the multicellular threshold will eventually be reached. It is possible that this species has no surviving offspring apart from the animal itself. To find more collateral offspring, one must push further back in time. The better the diversity of life that is sampled, the more likely a species will be found similar to what its ancestors wanted to reconstruct.
Billions of years old known as Holozoa consist of closely related unicellular animals and species, including choanoflagellates, filastereans, and ichthyosporeans. Only a decade ago this was an area of eukaryotic tree samples that were rarely sampled. For example, the first choanoflagellate genome was only published in 2008 (Brunet and King, 2017). At present dozens of holozoan species have been cultivated, sequenced and studied, and they are fertile hunting grounds for interesting cell biology.
Importantly, non-animal holozoans include species that can be temporary multicellular, at certain times or under certain conditions. In particular, some choanoflagellates and ichthyosporeans have multicellular clone life stages, while some filastereans form multicellular aggregates. But are these behaviors homologous with multicellularity in animals, and therefore represent ancestral conditions? Or are they examples of convergent evolution, driven by adaptation to a similar environment?
One way to answer this question is to solve the molecular mechanism that allows multicellular behavior in holozoans. Suggestively, the holozoan genome encodes transcription factors and cell adhesion genes that are known to be important for animal multicellularity, but the role of these genes has not been shown directly (Grau-Bové et al., 2017; Richter et al., 2018). Now, two independent teams have reported the results of studies of certain animal-like behavior in unicellular lineages that explain the evolution of animal multicellularity.
In a paper in eLife, Iñaki Ruiz-Trillo and colleagues from Barcelona, Liverpool, Oslo, Shizuoka and Hiroshima – including Omaya Dudin and Andrej Ondracka as joint authors – reported how reproduction in ichthyosporean was called Sphaeroforma arctica involves a growth stage that is reminiscent of the development of fruit fly embryos. The nucleus of the initial single cell divides repeatedly to form a polarized epithelial layer, which then gives rise to many cells when the membrane undergoes coordinated invagination (Dudin et al., 2019).
In the second paper at Science, Nicole King and coworkers from Berkeley and Amsterdam – including Thibaut Brunet, Ben Larson and Tess Linden as co-authors first – reported the results of research on the newly isolated choanoflagellate which they named Choanoeca flexa (Brunet et al., 2019). In bright light, these organisms exist as cup-shaped cell colonies, with their flagella pointing inward. However, in the dark, the cup flipped out through collective cellular contractions. This collective contraction is reminiscent of contractions that produce curvature in developing animal tissue.
Both studies use pharmacological imaging and inhibition to show that this multicellular process depends on the same molecular machinery: actin and myosin complexes that can produce mechanical strength in cells. These results indicate that the last ancestor of holozoans were organisms capable of temporary multicellularity, with cells that could contract collectively. Among their offspring, only animals that have evolved multicellular lifestyles permanently, use the power of collective contraction to carve out tissue and produce the "most beautiful endless forms" that greatly inspired Darwin.
This article was originally published by a journal eLife and has been republished here under the Creative Commons Attribution license.
Mukund Thattai is a faculty member of the National Center for Biological Sciences, part of the Fundamental Research Governance Institute. His research focuses on the evolution of complex cells.