One fish, two fish, red fish, stickleback

Last week an interesting paper on evolution in sticklebacks, a widespread mostly marine fish, was published in Nature. Sticklebacks are fascinating because populations have repeatedly become established in freshwater at various times since the last ice age. Because of this they provide an amazing system in which the processes of adaptive evolution and speciation can be investigated in the wild.

The threespine stickleback, Gasterosteus aculeatus.

Evolution is often defined as the change in allele* frequencies with time. Observations of evolution in the wild, such as previous studies on sticklebacks, show that adaptation to novel environments can happen surprisingly quickly (just 13 generations in one documented case). Too rapidly, some argue, for adaptive alleles to have arisen after the novel environment is encountered. But, the adaptive alleles may already be present in the population at low frequency.

The left image shows the skeletal differences between marine and freshwater sticklebacks. On the right are preserved specimens stained red. Note the strong divergence in morphology between the marine and freshwater forms, which can arise in just 13 generations (all images David Kingsley).

If sticklebacks adapted to freshwater through the selection of alleles that arose after they encountered the new environment, then alleles within freshwater populations should be most genetically similar to the populations they diverged form. Conversely, if adaptation occurred through selection on already existing alleles, then freshwater populations should share similar alleles with each other. And the authors tested which of these possibilities was operating in sticklebacks by sequencing the entire genome of ten pairs of sticklebacks. Each pair came from the same area, but one member was the marine form while the other was the freshwater form.

They then examined the genomes for regions that were similar among the marine or among the freshwater fish. Using two different statistical approaches to determine similarities among regions they found 242 regions (0.5% of the total genome) were identified by either test and 147 (0.2% of the total genome) that were identified by both were divergent between marine and freshwater fish. That is, just by looking at those regions in a given fish you could be reasonably confident about whether it lived in marine or freshwater.

Next the authors looked at the genes contained within the regions that were divergent between marine and freshwater sticklebacks. They found that there was a significantly higher density of genes within the identified regions that the genome overall. Then, using the 64 regions that showed the strongest differentiation between marine and freshwater fish, they looked at whether the genes coded for proteins or had a regulatory function. Regulatory genes modify the function of other genes via proteins or RNA.

Regulatory genes were more common within the 64 strongly divergent regions. Just 11 regions (17%) contained coding genes, while 26 regions (41%) were regulatory. The other 27 regions (43%) contained both coding and regulatory sequences, but in these regions none of the changes to coding genes produced different proteins. This strongly suggests that these regions have a principally regulatory effect on trait expression. Thus, regulatory changes account for a much higher proportion of the differences between marine and freshwater sticklebacks.

So, this study is really cool for two reasons. It shows that rapid adaptive evolution to a novel environment can be achieved using the genetic variation present in the parent population. And it shows that the regulation of when and where coding genes are expressed largely accounts for the for the differences between marine and freshwater populations. As the authors acknowledge, the next step is to determine which traits are affected by these genetic differences between marine and freshwater populations.

*Alleles are variants of genes.

Reference (open access!):

Jones, F., Grabherr, M., Chan, Y., Russell, P., Mauceli, E., Johnson, J., Swofford, R., Pirun, M., Zody, M., White, S., Birney, E., Searle, S., Schmutz, J., Grimwood, J., Dickson, M., Myers, R., Miller, C., Summers, B., Knecht, A., Brady, S., Zhang, H., Pollen, A., Howes, T., Amemiya, C., Baldwin, J., Bloom, T., Jaffe, D., Nicol, R., Wilkinson, J., Lander, E., Di Palma, F., Lindblad-Toh, K., & Kingsley, D. (2012). The genomic basis of adaptive evolution in threespine sticklebacks Nature, 484 (7392), 55-61 DOI: 10.1038/nature10944