Thursday, November 21, 2013

Is Baker's Yeast a Good Model for the Evolution of Multicellularity?

R. Ford Denison has an excellent blog called This Week in Evolution. He recently posted an article about the evolution of multicellularity [Evolving-multicellularity lab exercises]. That post contains a link to a paper he recently published with a former student (Ratcliff et al., 2013). Here's the abstract.
Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes.
Here's the problem. Most fungi are multicellular and Saccharomyces cerevisiae (budding yeast) almost certainly evolved from an ancestor that could form hyphae. In fact, wild-type diploid strains or Saccharomyces cerevisiae will form multicellular filaments (pseudohypha) in response to starvation for nitrogen (Liu et al., 1996).

Many of the common lab strains have lost the ability to form multicellular pseudohyphae because they carry a nonsense mutation in the FLO8 gene (Liu et al., 1996). Presumably, those strains have been selected by bakers and brewers over the past several thousand years.

In their discussion, Ratcliff et al. (2012) say ...
Although known transitions to complex multicellularity, with clearly differentiated cell types, occurred over millions of years, we have shown that the first crucial steps in the transition from unicellularity to multicellularity can evolve remarkably quickly under appropriate selective conditions.
I don't this this is quite fair since the yeast strain is just reverting to a primitive condition. This might only have required one or a few mutations. It's not a very good model for de novo evolution of multicellarity.

The work from Gerry Fink's lab (e.g. Liu et al. 1996) is a good example of why we should be cautious using yeast as a model for anything. The yeast strains used in the lab have been selected for specific characteristics since bread-making and beer-making were first invented over 4000 years ago. We need to be cautious about drawing general conclusions based on work with lab yeast strains.

The lab exercise based on the Ratcliff et al. (2012) paper [Experimental Evolution of Multicellularity] may be interesting but it's also misleading. The description of that experiment implies that students are reproducing the ancient evolution of multicellularity from single-cell organisms. Instead, what students are actually looking at is the reversion of a derived, exclusively single-cell strain, to the more primitive multicellular state. That's not the same thing.

[Photo Credit: That's Ford at a rally in Ottawa where we were protesting the Conservative government's clamp-down on science in Canada. He took advantage of the audience to advertise his book.

Liu, H., Styles, C.A. and Fink, G.R. (1996) Saccharomyces cerevisiae S288C has a mutation in FL08, a gene required for filamentous growth. Genetics 144:967-978. [PDF]

Ratcliff, W.C., Denison, R.F., Borrello, M. and Travisanoa, M. (2012) Experimental evolution of multicellularity. Proc. Natl. Acad. Sci. (USA) 109:1595-1600. [doi: 10.1073/pnas.1115323109]