Michel et al. 2010
Fri Jun 04 2010
Widespread genomic divergence during sympatric speciation
Speciation with gene flow is expected to generate a heteroge- neous pattern of genomic differentiation. The few genes under or physically linked to loci experiencing strong disruptive selection can diverge, whereas gene flow will homogenize the remainder of the genome, resulting in isolated “genomic islands of speciation.” We conducted an experimental test of this hypothesis in Rhagole- tis pomonella, a model for sympatric ecological speciation. Contra- ry to expectations, we found widespread divergence throughout the Rhagoletis genome, with the majority of loci displaying host differences, latitudinal clines, associations with adult eclosion time, and within-generation responses to selection in a manipulative overwintering experiment. The latter two results, coupled with linkage disequilibrium analyses, provide experimental evidence that divergence was driven by selection on numerous independent genomic regions rather than by genome-wide genetic drift. “Con- tinents” of multiple differentiated loci, rather than isolated islands of divergence, may characterize even the early stages of speciation. Our results also illustrate how these continents can exhibit variable topography, depending on selection strength, availability of preex- isting genetic variation, linkage relationships, and genomic fea- tures that reduce recombination. For example, the divergence observed throughout the Rhagoletis genome was clearly accentu- ated in some regions, such as those harboring chromosomal inver- sions. These results highlight how the individual genes driving speciation can be embedded within an actively diverging genome.
Speciation with gene flow is expected to generate a heteroge- neous pattern of genomic differentiation. The few genes under or physically linked to loci experiencing strong disruptive selection can diverge, whereas gene flow will homogenize the remainder of the genome, resulting in isolated “genomic islands of speciation.” We conducted an experimental test of this hypothesis in Rhagole- tis pomonella, a model for sympatric ecological speciation. Contra- ry to expectations, we found widespread divergence throughout the Rhagoletis genome, with the majority of loci displaying host differences, latitudinal clines, associations with adult eclosion time, and within-generation responses to selection in a manipulative overwintering experiment. The latter two results, coupled with linkage disequilibrium analyses, provide experimental evidence that divergence was driven by selection on numerous independent genomic regions rather than by genome-wide genetic drift. “Con- tinents” of multiple differentiated loci, rather than isolated islands of divergence, may characterize even the early stages of speciation. Our results also illustrate how these continents can exhibit variable topography, depending on selection strength, availability of preex- isting genetic variation, linkage relationships, and genomic fea- tures that reduce recombination. For example, the divergence observed throughout the Rhagoletis genome was clearly accentu- ated in some regions, such as those harboring chromosomal inver- sions. These results highlight how the individual genes driving speciation can be embedded within an actively diverging genome.