by Piter Kehoma Boll
Not long ago I talked about the peculiar genome of the freshwater planarian Schmidtea mediterranea and how it challenges our view of many cellular processes. Now what if I told you that planarians also challenge our view of what a multicellular organism is?
We all know that organisms may be either unicellular or multicellular, but sometimes it is hard to tell them apart, especially in what are called colonial organisms, in which clones of unicellular individuals may live together.
Green algae of the genus Volvox are somehow at the boundary between unicellular and multicellular organisms. Although usually considered a colony of unicellular organisms, they behave somewhat like a multicellular organism. Photo by Frank Fox.*
So where lies the boundary between gathered unicellular organisms and true multicellular organisms? One of the ideas is that for a group of cells to be considered a single unit (an organism) they must have high levels of cooperation and low levels of conflict between each other and, perhaps more important than that, they have to be dependent on the association in order to survive.
As most recent evolutionary theories predict, cooperation increases with genetic similarity. As a result, multicellular organisms are (almost) always composed of cells having the exact same genetic material, i.e., they are all clones. We know, however, that during DNA replication mutations may occur, so that eventually at least some cells of an adult and many-celled organism may have become genetically distinct. This leads to a need to find a way to fix this problem by reincreasing genetic similarity, and the way most organisms found to do that is by allowing only one lineage of their cells, the germ cells (which produce the gametes) to generate the next generation. Thus, each transition from one generation to the next passes through a “zygotic bottleneck”, i.e., a new organism is always generated from a single original cell, the zygote, which assures that the genetic similarity is always brought back.
A developing new egg, with an embryo that is created from a single original cell, the zygot, assuring a higher genetic similarity of the cells in the whole organism. Photo by Stéphanie Bret.**
The zygotic bottleneck is not a rule for a lot of species though. Many animals and plants are able to reproduce asexually by budding, fission or many other ways. In such cases, the new organism usually is built from several different lineages of the parent organism. For example, some succulent plants may generate a new organism from a dettached leaf and several cells of the original leaf start to reproduce and together they build the new plant and, as each lineage may have suffered different mutations, the offspring is not necessarily composed of genetically identical cells. Nevertheless, even such organisms, which are able to reproduce asexually, still retain the ability to generate zygotes through sexual reproduction, which eventually “cleans that mess”.
But in planarians things get really strange. First of all, let’s explain some basic things about planarians. They have, as you know, a remarkable regeneration ability. This happens due to the presence of stem cells called neoblasts that fill their bodies. Those neoblasts are able to generate all cell types that make up the planarian’s body. In fact, all cells in a planarian must come from neoblasts, because, as weird as it may be, all differentiated cells in a planarian body ARE UNABLE TO UNDERGO MITOSIS! Once a neoblast differentiates into any kind of cell, it is condemned to die in a few days without ever letting descendants. All cells in a planarian body are therefore constantly replaced by new ones coming from neoblasts. The only lineage of differentiated cells that is still able to reproduce is that of the germ cells, which, as in other multicellular organisms, assure that the next generation will consist of organisms with genetically homogeneous cells.
Girardia tigrina, a freshwater planarian. Photo by Wikimedia user Slimguy.**
Several freshwater planarians, however, have lost their ability to generate sexual organs and, as a result, germ cells. In order to reproduce, they must rely on a form of asexual reproduction, which in this case happens by transversal fission of the body and posterior regeneration of the missing parts. In these populations, the zygotic bottleneck disappeared completely and, as a result, any non-lethal mutation in the neoblasts is retained in the organism, leading to a population of genetically distinct neoblasts inside a planarian.
Therefore, considering the fact that asexual planarians are not genetically homogeneous, having several different neoblast lineages in the same body, and that the neoblasts are the only cells able to reproduce and continue the species, a recent publication by Fields and Levin (see references) suggests that asexual planarians are nothing more than a very complex environment built by neoblasts in order to survive. Considering that each neoblast is an independent cell, which only needs the environment (the planarian) to survive, but does not need other neoblasts, planarians, at least the asexual ones, do not seem to have reached completely the requirements of high internal cooperation and low internal competition to be considered multicellular organisms.
We could interpret the neoblasts as unicellular organisms that live together, cooperating to build a complex environment, the planarian body, with their own sterile descendants (the differentiated cells), as if they were a group of queen ants living among sterile castes. Kind of mind blowing, huh? But it actually makes sense.
If you want to read more about it and understand every detail in this theory, read the references below.
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Fields, C; Levin, M. (2018) Are Planaria Individuals? What Regenerative Biology is Telling Us About the Nature of Multicellularity. Evolutionary Biology: 1–11.
West, S. A.; Fisher, R. M.; Gardner, A.; Kiers, E. T. (2015) Major evolutionary transitions in individuality. PNAS 112 (33): 10112-10119. https://doi.org/10.1073/pnas.1421402112
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