Probing the evolution of surface-associated multicellularity

Surface-associated multicellular organisms are found throughout the biosphere and include common land plants, corals, lichens, bacterial biofilms and slime molds. Yet despite their prevalence, little is known about their origins.

University of Zürich researchers devised a novel approach to this problem using two-dimensional geometric simulations to try to reproduce the emergence and evolution of multicellularity. They focused on two properties of the cell as it moves on a surface: cell adhesion and what regulates that adhesion.

Their research appears in the May 13 edition of PLOS Biology.

The researchers describe how standard evolutionary theory, such as kin selection or multilevel selection theory, is difficult to use in this case because of the organisms' plasticity: The organisms "often display continuous growth, can merge, and adopt many different forms." The researchers also establish the principles of growth and reproduction of cells in surface colonization and model the problem from the bottom up.

The model uses a two-dimensional hexagonal grid, where each cell can have up to six neighbors. Each cell can be adhesive or be in association with an adhesive cell. A cell detaches if it loses adhesion.

The researchers then looked at initial cells, tracking them as they developed into collectives. Next, they looked at different scenarios of the probability of adhesion that can evolve through mutations.

Lineage tracking of individual cells allowed the researchers to probe collective formation while avoiding the problem of their cryptic appearance on the surface – where individual collectives often cannot be visually distinguished from each other.

The driving evolutionary force

Current Science Daily talked with Jordi van Gestel, lead author of the research paper and former postdoc student in the Department of Evolutionary Biology and Environmental Studies at the University of Zürich, Switzerland, where the work was performed. Van Gestel now works in the Department of Microbiology and Immunology, University of California, San Francisco. His co-author, professor Andreas Wagner, is an evolutionary biologist at the University of Zürich.

Van Gestel said that the general driving force for the evolution of surface-associated multicellularity is "the selective benefits of being in a good place, and it's visible in all kinds of organisms. If you think about beneficial places – for example, lichens on a tree like to be on the sunny side, or corals like to be close to the water surface. Organisms prefer to be in a better place, and surface attachment is a key factor there. So, if you manage to hole up in a place where there are sufficient nutrients or other resources, this is a driving force for surface-associated multicellularity."

Starting at the origin

In describing their research model, van Gestel said: "We start at the very origin of multicellularity. This is a different approach from that of other models. Its major benefit is that you can account for very primitive forms of development and self-organization. And those cannot be captured adequately with more classical models in which you assume certain groups to be present a priori and don't account for spatial organization."

He described the novel way they used spatial lineage tracking of cells, noting that "spatial lineage tracking of cells is not in itself novel, but it's novel in the way we use it. If you look at classical evolutionary theory, especially theory on the evolution of multicellularity, it's often based on the individual. And that makes sense because you have to explain how multi-celled individuals evolved. And what we typically do with those models is show what happens once cells form a group. This does not explain how those groups can originate in the first place and does not account for the fact that in reality those groups are often not readily identifiable.” 

"This hampered the study of surface-associated multicellularity," he said, "because groups in a primitive form cannot be recognized as such, or they're more difficult to recognize. And so instead we use spatial lineage tracking to allow us to study the primitive origins of multicellularity. That way we can trace those groups as they merge on the surface without needing any visual cues to distinguish those groups."

Asked about the trade-off between adhesion and reproduction in the research model, van Gestel said: "We modeled this in a generic way. Based on what we know from primitive multicellular organisms, we assume that if cells express adhesion, they have a lower rate of cell division. That's the key trade-off on the cellular level.

"And there's also an emergent trade-off at the collective level, which is apparent when many cells at the collective level express adhesion, then such a collective will produce fewer propagules, simply because the cell will remain attached to the surface."

The evolutionary picture

A big question we posed was how the research findings fit into the larger understanding of evolution, which van Gestel said was one of their "main fascinations."

"We are trying to merge knowledge about evolutionary biology and developmental biology," he said. "Ultimately if you want to explain the evolution of multicellularity, you have to explain how multi-cell development originates. Surprisingly, these fields have been fairly separated, until recently. 

"In the beginning of the 20th century, there was a branching point between evolutionary biology and developmental biology in which these disciplines were pursued separately. It's only recently--in the last decades--that these fields are again merging, like for example seen in evo-devo biology; this is a big field now. What we tried to do in our model is show how self-organizing systems originate. We therefore explicitly account for the interaction between cells, and model how these interactions give rise to primitive forms of development.

"Through our publication, we are helping to connect evolutionary biology and evolutionary theory to development biology and theory."

The power of multicellularity

Van Gestel said, "The finding we liked a lot in the model is that even very primitive forms of multicellularity can be very powerful. We show in the model that this kind of cell organization on the surface, which is not recognizable as multicellularity even from a distance, actually is a form of multicellularity that is cryptic, not visible. 

"It's interesting in respect to the vast number of organisms that colonize surfaces, that there might be very many organisms out there that have forms of multicellular organization that give them a huge competitive advantage that we now miss out on because we don't know how to properly study them." 

"And in any case," he concluded, "you cannot study them properly because we have a hard time culturing them in the lab. There is so much unexplored territory from our model in this direction in biology that will be great to explore."