Hunter B. Frasera,1,
Alan M. Mosesb, and
Eric E. Schadtc
-Author Affiliations
aDepartment of Biology, Stanford University, Stanford, CA 94305;
bDepartment of Cell and Systems Biology, University of Toronto, Toronto, ON M5S 3B2, Canada; and
cPacific Biosciences, Menlo Park, CA 94025
Edited by Jasper Rine, University of California, Berkeley, CA, and approved December 22, 2009 (received for review October 23, 2009)
Abstract
Changes in gene expression have been proposed to underlie many, or even most, adaptive differences between species. Despite the increasing acceptance of this view, only a handful of cases of adaptive gene expression evolution have been demonstrated. To address this discrepancy, we introduce a simple test for lineage-specific selection on gene expression. Applying the test to genome-wide gene expression data from the budding yeast Saccharomyces cerevisiae, we find that hundreds of gene expression levels have been subject to lineage-specific selection. Comparing these findings with independent population genetic evidence of selective sweeps suggests that this lineage-specific selection has resulted in recent sweeps at over a hundred genes, most of which led to increased transcript levels. Examination of the implicated genes revealed a specific biochemical pathway—ergosterol biosynthesis—where the expression of multiple genes has been subject to selection for reduced levels. In sum, these results suggest that adaptive evolution of gene expression is common in yeast, that regulatory adaptation can occur at the level of entire pathways, and that similar genome-wide scans may be possible in other species, including humans.
Footnotes
1To whom correspondence should be addressed: hbfraser@stanford.edu.
Author contributions: H.B.F. designed research; H.B.F. performed research; A.M.M. and E.E.S. contributed new reagents/analytic tools; H.B.F. analyzed data; and H.B.F., A.M.M., and E.E.S. 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/cgi/content/full/0912245107/DCSupplemental.
cPacific Biosciences, Menlo Park, CA 94025
Edited by Jasper Rine, University of California, Berkeley, CA, and approved December 22, 2009 (received for review October 23, 2009)
Abstract
Changes in gene expression have been proposed to underlie many, or even most, adaptive differences between species. Despite the increasing acceptance of this view, only a handful of cases of adaptive gene expression evolution have been demonstrated. To address this discrepancy, we introduce a simple test for lineage-specific selection on gene expression. Applying the test to genome-wide gene expression data from the budding yeast Saccharomyces cerevisiae, we find that hundreds of gene expression levels have been subject to lineage-specific selection. Comparing these findings with independent population genetic evidence of selective sweeps suggests that this lineage-specific selection has resulted in recent sweeps at over a hundred genes, most of which led to increased transcript levels. Examination of the implicated genes revealed a specific biochemical pathway—ergosterol biosynthesis—where the expression of multiple genes has been subject to selection for reduced levels. In sum, these results suggest that adaptive evolution of gene expression is common in yeast, that regulatory adaptation can occur at the level of entire pathways, and that similar genome-wide scans may be possible in other species, including humans.
Footnotes
1To whom correspondence should be addressed: hbfraser@stanford.edu.
Author contributions: H.B.F. designed research; H.B.F. performed research; A.M.M. and E.E.S. contributed new reagents/analytic tools; H.B.F. analyzed data; and H.B.F., A.M.M., and E.E.S. 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/cgi/content/full/0912245107/DCSupplemental.
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