Threespine sticklebacks are famous in the evolution world as a study system for rapid adaptation and speciation. In separate populations all over the world, they invaded from the ocean to adapt to the new freshwater environments created after the Pleistocene glaciers retreated about 11,000 years ago (evolutionarily speaking, this was very recent). This created naturally replicated marine/freshwater population pairs that still hybridize in nature. They even can be raised in a lab, which means they can also be experimented on. We know that all plants and animals have adapted to changing conditions at some point or another in their history, but the process is difficult to study in many organisms, and often the genomic signatures of such change are often obscured by the effects of too much time having passed. The sticklebacks have a perfect storm of attributes that make them great for studying these sorts of questions.
In a paper that begins by presenting the first threespine stickleback genome (which is exactly as far as many first genome papers go), Jones and collegues then go deeper into the system, using that genome to look in detail at how it responded to such recent and drastic environmental change. They leverage the power of the naturally replicated freshwater invasions by generating 20 additional genomes from marine/freshwater population pairs all over the world. In order to assess parallel changes occurring across the entire genome, they looked for regions in the genomes that were similar among all the freshwater animals worldwide but different from the marine ones. Using two complimentary approaches, they found 147 regions (0.2% of the whole genome) that were divergent among the ecotypes.
The researchers then focused in on one marine/freshwater population pair with an active hybrid zone to ask if these globally shared variants were the main ones involved or if there were also a lot of variants contributed by the local populations. They found of the divergent changes between the two populations, 35.3% contained these global variants, suggesting that there is a substantial contribution from local variants in each population in addition to what is shared across populations.
An outstanding question in biology asks whether adaptive changes occur because of changes in protein coding genes or regulatory regions. Evidence has been accumulating from a variety of systems about specific adaptations, which are typically restricted to relatively narrow regions within a genome. This study allowed a look at what is going on across an entire genome. The authors found that of all of the freshwater variants that were shared across all populations, 17% were located within protein coding regions, while 41% were found in non-coding regions and presumed to be regulatory. An additional 43% were more ambiguous, and the authors speculate that they also primarily fall into the regulatory category. More work needs to be done to classify and verify these variants, but the results are already suggestive that a significant amount of adaptive change across the genome is due to changes in the regulatory regions.
While we are not quite at a stage of being able to write a how-to manual on adapting to a novel environment, this series of studies provides a lot of new detail on how it works in nature in one particularly well-suited system – a system truly powerful and special for its ability to give us insight into the dynamics of rapid adaptation. Even though the et al on this paper is a long list of contributors that render this approach way beyond what is possible to do by a single researcher, it is still inspirational to picture how these approaches could illuminate the biology of other natural systems.
Jones, F.C. et al 2012. The genomic basis of adaptive evolution in threespine sticklebacks, Nature, vol 484, pp. 55-61. doi:10.1038/nature10944.