National Geographic

How I became we, which became I again

Most life on Earth exists as single cells. But the ones comprised of many cells, from the tiniest ant to the tallest tree, have had an undeniable impact on our planet. These ‘multicellular’ creatures evolved from single-celled ancestors at least 25 times throughout Earth’s history. These transitions are arguably some of the most significant in evolution, but we only have a vague understanding of how they happened.

It probably went a bit like this. A single cell split into two and rather than going their separate ways, they stayed together. This happened again and again. Eventually, the groups of individual cells became individuals of grouped cells, evolving as a unit. It’s the story of how I became we, and how we became I again.

In an elegant new experiment, William Ratcliff from the University of Minnesota has shown that this story could have been a surprisingly quick one. In his laboratory, he successfully nudged single-celled brewer’s yeast into multicellular clusters, within just a few months. The clumps of cells evolved as one. They even developed a primitive division of labour, with some of them deliberately dying so that the others could grow and reproduce.

I’ve written about this discovery for Nature News, so head over there to read the full take.

Over here, I want to emphasise that Ratcliff’s work isn’t meant to directly recap how multicellularity evolved in any particular group. It’s meant to look at the general principles that govern this transition. Richard Lenski, another evolutionary biologist famous for his work on bacteria, adds, “They’re not saying that it happened in nature the way it happened in their experiments. The point of experimental evolution is to test hypotheses and watch evolution in action, not to replicate a specific event from some point in the distant past.”

Ratcliff’s work shows that this transition, from one cell to many, could have happened much more quickly than anyone expected. To set his yeast along that path, all he had to do was to let them sink. In a tube of liquid, clumps of yeast will settle faster than single cells. By picking and growing the cells that sunk quickest, Ratcliff selected for those that tend to stick together.

Many single-celled microbes clump together to create multicellular entities, from predatory bacteria like Mxyococcus to slime moulds like Dictyostelium. Yeast cells sometimes do this too – they form clumps called ‘flocs’. Ratcliff says, “My original guess was that we flocculation would evolve, but that’s not what we saw.”

Within 60 days, the yeast had evolved clusters of many cells, radiating out into microscopic ‘snowflakes’. Unlike flocs, these flakes weren’t clumps of unrelated cells. They were formed by genetically identical cells that grew and divided, but never separated. That’s similar to what happens in our own bodies. A single cell – a fertilised egg – grows and divides into trillions of cells that all stay together.

Many other studies have shown that sticking together would have provided benefits for single cells. “We can be fairly confident that, early on, large size was beneficial”, says Ratcliff. In a cluster, single cells are better at absorbing nutrients from their environment, surviving through rough conditions, or escaping predators.

But these studies only hint at the conditions that encourage cells to stay in groups. Ratcliff’s experiments speak to something subtler and more important: the transition from groups of distinct cells to true multicellular individuals. That’s what his snowflakes were. As I write in the Nature piece:

The snowflakes behaved like true multicellular organisms. They had a simple life cycle with a juvenile stage, when they grew unimpeded, and an adult one, when they reached a certain size and split into a large parent flake and a smaller, daughter flake.

Ratcliff could even tune these stages. If he cultivated only those snowflakes that settled faster, he ended up with larger ones that grew bigger before splitting. This confirmed that natural selection was acting on the entire flake, rather than on the individual cells within it. “They survive as a whole, or they die as a whole. Selection shifts to the multicellular level,” says Ratcliff.

The snowflakes split because some of their component cells sacrifice themselves, allowing pieces to snap off. These individual cells die for the good of the whole, allowing the parent flake to continue growing and produce many offspring.

This mirrors a critical division in other multicellular creatures, such as us, between two groups of cells – the soma (body) and the germline. Lenski explains the difference well: “The vast majority of cells in our bodies are soma, and those cells won’t live beyond our individual mortal existence.  But the germline cells produce the sperm and eggs. Through reproduction, these privileged cells are, in some sense, immortal. Their lineages can go on and on, even after we die, so long as the bodies they build from fertilized eggs survive to reproduce in each generation.” The same is true for the yeast snowflakes. The dying cells are like the soma, and the surviving ones are like the germline.

Reference: Ratcliff, Denison, Borrello & Travisano. 2011. Experimental evolution of multicellularity. PNAS http://dx.doi.org/10.1073/pnas.1115323109

Images and video by Will Ratcliff

There are 9 Comments. Add Yours.

  1. Tim Martin
    January 16, 2012

    In a cluster, single cells are better at… what?! I must know! (aka, your last sentence needs finishing.)

    Also, where is the link to your piece at Nature News?

  2. nolan
    January 16, 2012

    The reason they cluster is that in the experiment they always got rid of the floaters. The yeast then evolved into multiple cell organizm so that it would be heavier and sink faster. More cells, heavier organism. Heavier organisms sink faster. The faster it sinks, the more likely it is to survive in this scenario.

  3. Alex Wild
    January 16, 2012

    Oh, mad libs! I love mad libs.

  4. Leonid
    January 16, 2012

    It’s been shown that incomplete daughter cell separation after division is the common, ancestral state in wild S. cerevisiae yeast, and that lab strains show single-cell growth due to a lab-acquired mutation in the gene AMN1, which normally inhibits daughter cell separation. Presumably, this mutation was artificially selected by early yeast researchers because it made it easier to streak for single colonies. Known mutations in AMN1, ACE2, and CTS1, among others, can “toggle” yeast between growth as single colonies and growth as larger clumps of cells formed due to incomplete mother-daughter separation.

  5. Jess Tauber
    January 16, 2012

    Add a couple of nanoprocessors that the cells themselves can manufacture, put them through the selectional wringer, and, TADAAA! Grey Goo. Run for the hills, because it ain’t gonna discriminate between Republicans, Democrats, or marmots.

  6. Adam B
    January 16, 2012

    The missing text (URL encoded in the HTML through the magic of a smartquote replacing a normal quote):
    Single cells are better at…

    …absorbing nutrients from their environment, surviving through rough conditions, or escaping predators.

    But these studies only hint at the conditions that encourage cells to stay in groups. Ratcliff’s experiments speak to something subtler and more important: the transition from groups of distinct cells to true multicellular individuals. That’s what his snowflakes were. As I write in the Nature piece:

    The snowflakes behaved like true multicellular organisms. They had a simple life cycle with a juvenile stage, when they grew unimpeded, and an adult one, when they reached a certain size and split into a large parent flake and a smaller, daughter flake.

    Ratcliff could even tune these stages. If he cultivated only those snowflakes that settled faster, he ended up with larger ones that grew bigger before splitting. This confirmed that natural selection was acting on the entire flake, rather than on the individual cells within it. “They survive as a whole, or they die as a whole. Selection shifts to the multicellular level,” says Ratcliff.

    The snowflakes split because some of their component cells sacrifice themselves, allowing pieces to snap off. These individual cells die for the good of the whole, allowing the parent flake to continue growing and produce many offspring.

    This mirrors a critical division in other multicellular creatures, such as us, between two groups of cells – the soma (body) and the germline. Lenski explains the difference well: “The vast majority of cells in our bodies are soma, and those cells won’t live beyond our individual mortal existence.  But the germline cells produce the sperm and eggs. Through reproduction, these privileged cells are, in some sense, immortal. Their lineages can go on and on, even after we die, so long as the bodies they build from fertilized eggs survive to reproduce in each generation.” The same is true for the yeast snowflakes. The dying cells are like the soma, and the surviving ones are like the germline.

  7. Brian Schmidt
    January 17, 2012

    This experiment and the evolution of multicellularity 25 times have implications for the Rare Earth hypothesis, which posits that microbial life is common in the galaxy but complex life isn’t. I think they have to change their theory from complex life to large, complex life is uncommon. That starts to make it look somewhat patched together.

  8. Ed Yong
    January 17, 2012

    Brian – it doesn’t actually impact the Rare Earth hypothesis. The reason why they think that complex life is uncommon is not because multicellularity is hard to evolve, but because complex eukaryote-equivalent cells are hard to evolve. The idea is that such cells are a product of a very rare and very accidental partnership between two prokaryotes. Only as a result of that partnership can you evolve a more complicated type of cell with the energy requirements needed to get multicellular and big. Note that yeast are already eukaryotes. Getting from a single-celled eukaryote to a multi-celled one may be easier than we thought, but getting from a prokaryote to a eukaryote is still very very challenging.

  9. Catherine Crawley
    January 25, 2012

    A study published in 2010 in PLOS Computational Biology demonstrated this rapid rise of multicellular organisms in a mathematical model. The transition from colonies of individual cells to multicellular organisms can be achieved relatively rapidly, within one million generations. Using germ and soma cells in volvocacean green algae, the model describes the evolutionary emergence of the division of labor starting with a colony of undifferentiated individual cells and ending with completely differentiated multicellular organisms. It is the first model to show the evolution of complete germ-soma differentiation, where one part of the colony’s cells (germ) eventually specializes in reproduction and the other part of the colony’s cells (soma) specializes in survival. Division of labor can occur if two conditions are met: there must be strong genetic relatedness and fitness trade-offs preventing individual cells from performing multiple functions efficiently.
    Citation is here: Gavrilets S (2010) Rapid Transition towards the Division of Labor via Evolution of Developmental Plasticity. PLoS Comput Biol 6(6): e1000805. doi:10.1371/journal.pcbi.1000805. A summary of the study is here: http://www.eurekalert.org/pub_releases/2010-06/plos-mer060810.php

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