Andrew P. Michel a,1, Sheina Sim a, Thomas H. Q. Powell a, Michael S. Taylor a,2, Patrik Nosil b,c, and
Jeffrey L. Feder a,b,3
-Author Affiliations
aDepartment of Biological Sciences, University of Notre Dame, South Bend, IN 46556-0369;
bInstitute for Advanced Study, Wissenschaftskolleg, Berlin 14193, Germany; and
cDepartment of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309
↵1Present address: Department of Entomology, Ohio State University, Wooster, OH 44691.
↵2Present address: Department of Biology, Southeast Missouri State University, Cape Girardeau, MO 63701.
Edited by Douglas Futuyma, Department of Ecology and Evolution, State University of New York, Stony Brook, NY, and approved April 19, 2010 (received for review January 26, 2010)
Abstract
Speciation with gene flow is expected to generate a heterogeneous 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 inRhagoletis pomonella, a model for sympatric ecological speciation. Contrary to expectations, we found widespread divergence throughout the Rhagoletisgenome, 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. “Continents” 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 preexisting genetic variation, linkage relationships, and genomic features that reduce recombination. For example, the divergence observed throughout the Rhagoletisgenome was clearly accentuated in some regions, such as those harboring chromosomal inversions. These results highlight how the individual genes driving speciation can be embedded within an actively diverging genome.
host race inversion island of speciation latitudinal cline Rhagoletis pomonella
Footnotes
3To whom correspondence should be addressed. E-mail: jfeder@nd.edu.
Author contributions: A.M., T.P., and J.F. designed research; A.M., S.S., T.P., M.T., and J.F. performed research; A.M., T.P., P.N., and J.F. analyzed data; and A.M., P.N., and J.F. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1000939107/-/DCSupplemental.
3To whom correspondence should be addressed. E-mail: jfeder@nd.edu.
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