Parallel Adaptive Evolution and Genomic Changes in Stickleback Fish

Contributed by: Jongmin Nam

            The molecular basis of phenotypic evolution is largely unknown, and identification of exact DNA changes underlying a specific morphological, physiological, or behavioral evolution is very hard, though it is a fascinating subject. Despite these difficulties, stickleback fish have been a great model system for studying the molecular basis of adaptive evolution, because they have experienced rapid parallel adaptation from salt to freshwater life in multiple geographical locations. They are therefore good organisms for studying recurrent adaptive evolution.

             In a recent Nature paper, Jones et al. (1) sequenced the genomes of multiple, independently evolved marine-freshwater pairs of sticklebacks (see Figure 1). They then examined sequence changes that are shared by most freshwater fishes but are different from typical sequences shared by most saltwater fishes. Not only did they detect what was already known, but they also detected about 60 strong candidate genomic regions for recurrent adaptive evolution. About 40% - 80% of them had either changes in noncoding regions or synonymous substitutions in protein coding regions, and only about 17% contained changes causing amino acid substitutions. Genes within or near these protein-coding regions varied widely from differentiation genes to regulatory genes. It would be of great interest to study molecular function of these regions in relation to the changes of specific phenotypic characters.

Figure 1. Genome scans for parallel marine–freshwater divergence. Marine (red) and freshwater (blue) stickleback populations were surveyed from diverse locations.

           

            Conducting killer experiments to show causality of these regulatory changes to specific phenotype evolution is still challenging, partly because we do not know how these functional elements work in complex regulatory networks and partly because experimental tools for re-engineering functional elements in the genome are not yet available in most species. Nevertheless, there are at least a good number of candidate regions for studying adaptive evolution to begin with, and this is a big step forward.

Abstract Marine stickleback fish have colonized and adapted to thousands of streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high-quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of twenty additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine–freshwater divergence. Our results indicate that reuse of globally shared standing genetic variation, including chromosomal inversions, has an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine–freshwater evolution, but regulatory changes appear to predominate in this well known example of repeated adaptive evolution in nature.

References

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