Molecular Mechanisms of Adaptive Divergence and Speciation


What is the molecular basis of adaptive trait variation? How do new species evolve? What genes, mutations, molecular and developmental mechanisms underlie adaptation to divergent environments?

The threespine stickleback fish is an excellent organism to study the molecular mechanisms of adaptation and speciation in vertebrates: >250 whole genome sequences, a powerful suite of genetic tools (eg transgenic manipulation, genome editing), and diverse natural populations with rapidly evolving adaptive phenotypes. We leverage natural evolutionary replicates to functionally dissect the molecular mechanisms & evolutionary processes that give rise to adaptive traits and biodiversity.

Whole genome analysis of parallel divergent stickleback ecotypes has resulted in one of the highest resolution maps of adaptive loci in vertebrates (Jones et al Nature, 2012). The majority of adaptive loci are intergenic (non-coding) and in regions of low recombination. This suggests the mutations in regulatory sequence and the recombination landscape are important in adaptive evolution. How do these mutations affect phenotype and fitness? How do recombination ’hot’ & ’cold’ spots vary across the genome? What are the factors that constrain and promote the availability of adaptive genetic variation in naturally evolving populations?

We aim to:

    1) genetically dissect and functionally test adaptive mutations using genetic and transgenic techniques (enhancer assays, genome editing, QTL mapping)

    2) molecularly dissect the genomic recombination landscape and mechanisms of recombination suppression

    3) use bioinformatic analyses of hundreds of whole genome sequences to identify and characterize selective sweeps across the genome

    4) combine empirical population genomic data with theoretical models of selection-migration balance and selective sweeps to test factors constraining and promoting adaptation in natural populations.


Whole genome sequencing of 21 marine and freshwater populations around the world revealed high resolution signals of marine-freshwater adaptive divergence - candidate genes for contributing to reproductive isolation

Example of Tol2 transgenic gain-of-function assay: Cardio myosin light chain promoter drives expression of green fluorescent protein in the developing heart of a three spine stickleback. The threespine stickleback has undergone an adaptive radiation in the last 10,000-20,000 generations resulting in a diversity of forms including parallel reproductively isolated species-pairs. These provide valuable biological replicates of the evolutionary process


Our research is funded by the Max Planck Society, a European Research Council Consolidator Grant, the Deutsche Forschungsgemeinschaft, an Alexander von Humboldt Foundation Postdoctoral Fellowship to Dr Saad Arif and an Human Frontier Science Program Fellowship to Dr Enni Harjunmaa.


Selected Publications

1.    Jones FC*, Grabherr MG*, Chan YF*, Russell P*, Mauceli E, Zody MC, Pirun M, Johnson J, White S, Birney E, Searle S, Schmutz J, Grimwood J, Dickson MC, Myers RM, Miller CT, Summers BR, Knecht AK, Brady, SD, Zhang H, Pollen AA, Howes T, Amemiya C, Broad Whole Genome Sequencing Platform and Whole Genome Assembly Team, Lander ES, DiPalma F, Lindblad-Toh K, and Kingsley DM.  (2012)  The genomic basis of adaptive evolution in threespine sticklebacks.  Nature 484:55-61.

2.    Jones FC, Chan YF, Schmutz J., Brady SD, Southwick A, Myers RM, Schluter D, & Kingsley DM.  (2012)  A genome-wide genotyping array reveals patterns of global and species-pair divergence in threespine stickleback.  Current Biology 22, 794-800.

3.    Chan YF, Marks ME, Jones FC, Villarreal G Jr, Shapiro MD, Brady SD, Southwick AM, Absher, DM, Grimwood J, Schmutz J, Myers RM, Petrov D, Jonsson B, Schluter D, Bell MA & Kingsley DM.  (2010)  Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer.  Science 327 (5963): 302-305.

4.    Kitano J, Ross JA, Mori S, Kume M, Jones FC, Chan YF, Absher DM, Grimwood J, Schmutz J, Myers RM, Kingsley DM & Peichel CL.  (2009)  A role for a neo-sex chromosome in stickleback speciation.  Nature 461, 1079-1083.

5.    Jones FC, Brown C, Pemberton JM & Braithwaite VA.  (2006)  Reproductive isolation in a threespine stickleback hybrid zone.  Journal of Evolutionary Biology 19 (5), 1531-1544.

see full publication list here