In a previous blog post, Andrew outlined the “ideal approach” for investigating whether plasticity facilitates evolution, and to my delight, he proposed experimental evolution. Not only that, but he proposed the experiment my group got published this week in Proceedings B. I was pleased to be accused of doing anything ideal, much less an ideal experiment, even if Andrew doesn’t seem to remember me presenting this very data at the American Genetics Association Meeting.
When Elisa Schaum (the PhD student behind all this work) and I planned this experiment 3 years ago, our main concern was that it was, if anything, too obvious: in order to test whether plasticity facilitates evolution, take plastic and non-plastic populations, put them in new environments, and watch them evolve. Not so easy if you study elephants, but completely doable if you study microalgae (like we do).
To conduct our “ideal experiment” (do I like the sound of that too much?), we used plastic and non-plastic isolates of the small but mighty marine picoplankton Ostreococcus. Ostreococcus is exciting for many reasons, among them that it is the smallest known free-living eukaryote and yet manages to house a huge virus. However, we chose it mostly because it is distributed over most of the world’s oceans, and we supposed that Ostreococcus from different locations would differ in how plastic they were in their response to CO2 enrichment (we were right, and we published this in Nature Climate Change). We used 16 different isolates of Ostreococcus from different locations. We found that isolates from environments with more variable and less predictable CO2 levels showed the largest plastic response to changes in CO2, meaning that we had plastic and non-plastic (and intermediately plastic) genotypes of Ostreococcus.
Two TEM images of Ostreococcus. Photos: C.E. Schaum.
Then, we set up the evolution experiment. We let all of the genotypes evolve in 4 different environments. First, we used a control environment where CO2 levels were normal and stable. Second, we used a fluctuating environment, where mean CO2 levels were the same as the control, but they fluctuated around this mean every few generations – we hypothesized that this environment would select for plasticity, but not for adaptation to high CO2. Third, we used a stable high CO2 environment, where we could look at how the initial plasticity of the genotypes affected evolution in a new environment even if there was no further need for plasticity. Finally, we used a fluctuating high CO2 environment, where mean CO2 levels were high, but also fluctuated every few generations, to look at how plasticity affected evolution in a new environment when there was also selection for plasticity. Then, we let everything evolve for a few hundred generations. We are now up to 1000 generations in the lab, but the paper was written before we reached this point of insanity.
Aaaannnnnd… plasticity facilitates evolution. Genotypes that were more plastic evolved more in high CO2 environments. Not only that, but populations in fluctuating high CO2 environments evolved more than populations in stable high CO2 environments. And to make matters even more exciting, populations evolved in fluctuating environments were more plastic than populations evolved in stable environments, no matter what the level of CO2. So, even when plasticity itself is selected for, populations evolving in response to an environmental change still evolve faster than populations dealing with that same environmental change who don’t have to bother with selection for plasticity. I may have done a happy dance when I saw that data.
Dr. Collins expressing her love for Osteococcus, post-results. Photo: Jane Charlesworth. [We tried to obtain a video of the good-data happy dance, but it was not available at press time. – The Management]
Of course, things are never that simple. The evolutionary response of Ostreoccocus to high CO2 can only be described as weird. I think this is because CO2 is food for many photosynthetic organisms, including Ostreococcus. So, when CO2 levels increase, Ostreococcus cells divide faster. This means that working with high CO2 here is at odds with the usual way of doing an evolution experiment with microbes, where researchers generally starve, poison, overheat, or do some other horrible thing to decrease microbial fitness substantially at the beginning of the experiment. However, we discovered that we were (eventually, and inadvertently) also guilty of torturing our microbes, as it turns out that a higher growth rate is all well and fine for a few generations for Ostreococcus, but after a while, dividing so quickly takes a toll, and the cells become less able to survive the slings and arrows of outrageous fortune (heat), have leaky mitochondria, and are bad at competing against other Ostreococcus. So, the evolutionary response to high CO2 in Ostreococcus – the response that results in cells that have normally-functioning mitochondria, can handle a bit of heat, and can overgrow other genotypes – is to grow more slowly. Basically, evolution reverses the plastic response to high CO2. Even though cells grow faster in the short term in high CO2 environments, they slow back down again if given enough time to evolve. Most theory for evolutionary biology isn’t tested in enriched environments, so it took us a while (and quite a few cups of hot chocolate) to figure that out.
So yes, I would say that the experiment was ideal. It had everything: tiny protagonists (Ostreococcus), clear results (plasticity facilitates evolution!), weird and surprising twists in the clear data (evolving slower growth than your own ancestor!), and a happy dance (possibly two).
Sinéad Collins and Elisa Schaum
Institute of Evolutionary Biology, University of Edinburgh
Proceedings B paper: http://rspb.royalsocietypublishing.org/content/281/1793/20141486.full
Nature Climate Change paper: http://www.nature.com/nclimate/journal/v3/n3/full/nclimate1774.html