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Test Tube Yeast Evolve Multicellularity

By watching evolution in progress, scientists reveal key developments in the evolution of complex life and put evolutionary theories to the test



William Ratcliff

The transition from single-celled to multicellular organisms was one of the most significant developments in the history of life on Earth. Without it, all living things would still be microscopic and simple; there would be no such thing as a plant or a brain or a human. How exactly multicellularity arose is still a mystery, but a new study, published January 16 in Proceedings of the National Academy of Sciences, found that it may have been quicker and easier than many scientists expected.

"This is a significant paper that addresses one of the most fundamental questions in evolutionary and developmental biology," says Rick Grosberg, an evolutionary biologist at the University of California, Davis, who was not involved with the research.

Since evolution acts on individual cells, it pays off for a cell to be selfish. By hogging resources and hindering neighbors, a cell can increase the odds that more of its own genes get passed into the next generation. This logic is one of the reasons it has been challenging to imagine how multicellularity arose; it requires the subjugation of self-interest in favor of the group’s survival.

"Traditional theories make this out to be a difficult transition because you have to somehow turn off selection on the individual cells and turn it on for the collective," says Carl Simpson, a paleobiologist at the Museum für Naturkunde in Berlin, who also was not involved in the research. "The big result here is that these transitions can be super easy."

In the new paper, researchers at the University of Minnesota used a simple but elegant technique to artificially select for multicellularity in yeast. They dumped unicellular yeast into a tube of liquid food and waited a few minutes for the cells to settle. Then they extracted the lowest fraction of the liquid and allowed whatever cells it contained to form the next generation. Because the cells had to cluster together in order to sink to the bottom and survive, the artificial selection made it more advantageous for yeast to cooperate than to be solitary.

After just 60 generations, all of the surviving yeast populations had formed snowflake-shaped multicellular clusters. "Hence we know that simple conditions are sufficient to select for multicellularity," says biologist Michael Travisano, who led the research.

But at what point do the yeast become something more than a cluster of cells? When do they begin behaving as one organism?

In a true multicellular organism, such as a rabbit, evolution acts on the rabbit and not on each of the billions of cells that build it. So the researchers set out to determine whether artificial selection would act on the snowflake yeast as if they also were multicellular organisms. To test it, one batch of the multicellular yeast was allowed only five minutes to settle in a tube (representing a strong selection pressure), whereas another batch was given 25 minutes (a weaker selection pressure). After 35 generations, the yeast that were exposed to stronger selection evolved to have larger cluster sizes, whereas those in the weak selection group actually shrank in size. This indicated that each cluster of cells was evolving as one organism.

In addition, time-lapse photography (video below) revealed that, in order to reproduce, the multicellular yeast divides itself into branches that develop into the multicellular form as well. The daughter clusters did not create their own offspring until they had reached a similar size as their parents. The presence of this juvenile stage shows that the snowflake yeast had adopted a multicellular way of life, says William Ratcliff, a postdoctoral student in Travisano’s lab.

 

The researchers also found evidence of rudimentary division of labor, which is an essential characteristic for more complex multicellular life forms. In a human, for example, some cells may differentiate into blood cells, others may differentiate into immune cells, but only select egg or sperm cells help form the next generation.

In the multicellular yeast, the division of labor was more subtle. Although the experiment's artificial selection favored large clusters, a large cluster required more time to grow before it could reproduce. That meant that smaller clusters, which divide in half more quickly, could soon outnumber the larger clusters. But after many generations of selection, the large clusters evolved a solution: nonreproductive cells which served as points where offspring could break away from the parent cluster. By providing more break points, these specialized cells allowed the clusters to break into more pieces, to produce a greater number offspring quickly.

“The discovery that there are cells specialized to die in order for the structure to reproduce is suggestive of the first steps toward cellular differentiation,” Grosberg says.

Although researchers agree that the yeast clusters could indeed be considered multicellular organisms, they remain relatively simple. "The researchers are not going to evolve sponges with this approach, but it's amazing what they’re able to do so quickly," Simpson says.

The fast evolution was not all that surprising to Grosberg, who has written papers arguing that multicellularity should be relatively easy to evolve; other researchers have estimated that multicellularity has arisen independently on at least 25 different occasions throughout the history of life. Yet nobody really knew how it originated, or what steps were involved in the process. By watching evolution in progress, the new research uncovered experimental evidence for these theories and revealed one possible scenario of how multicellularity may have evolved.

"We had hypotheses about how multicellularity could evolve, but until now, no one has really been able to test them,” Ratcliff says. "Now that we have this experimental system, we can ask lots of really exciting questions."

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