Watching multicellularity evolve before our eyes

Chlorella vulgaris is an asexual, unicellular green alga. It has been observed in the laboratory to maintain unicellularity for thousands of generations. Boraas and his collaborators (1998) kept Chlorella for two decades in this way. Then they decided to add a predator, Ochromonas vallescia, also a unicellular organism. It has a flagellum (a tail with which it can swim about), and it eats Chlorella. This is bad news for the Chlorella population, which thus experiences a shift in selective pressure. While it was previously adapted to maximize growth by uptake of nutrients, with Ochromonas around it is suddenly more advantageous to have some sort of defense, even if that should come at a cost of the rate at which it can reproduce.

While we could imagine other mechanisms of defense, size is an obvious choice. Very soon (about 10 days) after the introduction of the flagellate predator, Chlorella colonies started to form. These initially consisted of aggregates of tens to hundreds on Chlorella cells, adhering to each other. Their sheer size prevented the predator from eating them, and thus the multicellular Chlorella was fitter than the unicellular ones, and as a result the unicellular Chlorella all but disappeared. Multicellularity had evolved right before the lucky scientists' eyes.


Single Chlorella cell (FC), Chlorella colony (CC), and the flagellate predator, Ochromonas (Oc) with its flagellum (Fl).

Recall that Chlorella is better able to utilize the nutrients in the environment when they are single cells. Thus, the colonies of tens to hundreds of cells soon disappeared, replaced by colonies of of only eight cells. This seems to be the optimal size for uptake of nutrients and defense against Ochromonas. When Boraas et al. removed the predator from the environment, Chlorella colonies continued to make multicellular offspring. However, with the selection pressure to be large gone, the unicellular Chlorella took over again.

The significance of this experiment is that it lends support to the hypothesis that a predator-prey arms race could provide the needed environmental change to enable multicellular organisms to evolve. It also is an outstanding example of observed evolution in the laboratory. It can be argued that the unicellular and multicellular Chlorella are different species, and this is then also an example of speciation observed.

Now contrast this Chlorella with the famous E. coli experiment by Blount et al. reported in PNAS this year. In short, after years of culturing E. coli bacteria in the lab, they one day evolved the capacity to metabolize a new nutrient, citrate. Scientists use E. coli's inability to metabolize citrate to distinguish it from other bacteria, so the fact that they suddenly evolved the ability to eat it can also be argued to be an instance of speciation.

However, there is a clear difference from Boraas' experiment, namely that Chlorella evolved almost instantly when the selection pressure changed. It thus responded to the change on the basis of standing genetic variation: different genotypes present in the population. There were already some Chlorella cells that were able to adhere to their daughter cells, but it was unfavorable to do so until the appearance of predators. In Blount's experiment it was always favorable to consume citrate. There was plenty of it, and E. coli was deliberately starved on its usual nutrient. Yet they had to wait 30 years to observe E. coli evolving to eat citrate, because the genetic components enabling them to do so had to evolve first. A yet unknown sequence of necessary mutations was required, and once it appeared, E. coli speciated.

References:
Martin E. Boraas, Dianne B. Seale, Joseph E. Boxhorn (1998). Phagotrophy by a flagellate selects for colonial prey: A possible origin of multicellularity Evolutionary Ecology, 12 (2), 153-164 DOI: 10.1023/A:1006527528063

Z. D. Blount, C. Z. Borland, R. E. Lenski (2008). Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli Proceedings of the National Academy of Sciences, 105 (23), 7899-7906 DOI: 10.1073/pnas.0803151105

The Chlorella experiment is referenced in chapter 7 of Your Inner Fish by Neil Shubin.