The genomic basis of adaptive evolution in threespine sticklebacks

We develop a high-quality reference genome assembly for threespine sticklebacks

Felicity C. Jones; Broad Institute Genome Sequencing Platform & Whole Genome Assembly Team; Manfred G. Grabherr; Yingguang Frank Chan; Pamela Russell; Evan Mauceli; Jeremy Johnson; Ross Swofford; Mono Pirun; Michael C. Zody; Simon White; Ewan Birney; Stephen Searle; Jeremy Schmutz; Jane Grimwood; Mark C. Dickson; Richard M. Myers; Craig T. Miller; Brian R. Summers; Anne K. Knecht; Shannon D. Brady; Haili Zhang; Alex A. Pollen; Timothy Howes; Chris Amemiya; Eric S. Lander; Federica Di Palma; Kerstin Lindblad-Toh; David M. Kingsley


Scholarcy highlights

  • 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
  • Using genotyping assays for single nucleotide polymorphisms in 11 regions recovered by both self-organizing map-based iterative Hidden Markov Model and cluster separation score analyses, we found that 91% of tested regions show significant enrichment of ecotypic alleles in independent marine and freshwater populations
  • The signal resolution of repeatedly used adaptive loci approaches,5 kb, often identifying single genes or intergenic regions, and offering a significant advantage over the several hundred kilobase candidate intervals typically identified in genetic mapping crosses, or the megabase or larger regions identified in previous selection scans of the stickleback genome
  • The many marine–freshwater divergent loci and gene expression changes identified in the current study will substantially accelerate ongoing searches for the genetic and molecular basis of fitness-related morphological, physiological and behavioural differences between marine and freshwater fish
  • Our results indicate that parallel evolution of marine and freshwater sticklebacks occurs by dynamic reassembly of many ‘islands’ of divergence distributed across many chromosomes
  • The larger fraction of regulatory changes implicated during repeated stickleback evolution may reflect our use of whole-genome rather than candidate gene approaches, stronger selection against loss-of-function and pleiotropic protein-coding changes in natural populations than in laboratory or domesticated organisms, or an increasing prevalence of regulatory changes at interspecific compared to intraspecific levels, including emerging species such as marine and freshwater sticklebacks
  • Given the considerable fraction of parallel stickleback evolution probably occurring by shared variants, sequencing of additional populations should make it possible to identify shared loci contributing to other ecological traits, again using the power of replicated evolution to illuminate both specific and general mechanisms underlying evolutionary change in natural populations

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