James H. Bullard a, Yulia Mostovoy b, Sandrine Dudoit a,c, and Rachel B. Brem b,1
-Author Affiliations
aDivision of Biostatistics,
bDepartment of Molecular and Cell Biology, and
cDepartment of Statistics, University of California, Berkeley, CA 94720
Edited* by David Botstein, Lewis-Sigler Institute, Princeton, NJ, and approved February 1, 2010 (received for review November 10, 2009)
Abstract
The search to understand [SIC] how genomes innovate in response to selection dominates the field of evolutionary biology. Powerful molecular evolution approaches have been developed to test individual loci for signatures of selection. In many cases, however, an organism's response to changes in selective pressure may be mediated by multiple genes, whose products function together in a cellular process or pathway. Here we assess the prevalence of polygenic evolution in pathways in the yeasts Saccharomyces cerevisiae and S. bayanus. We first established short-read sequencing methods to detect cis-regulatory variation in a diploid hybrid between the species. We then tested for the scenario in which selective pressure in one species to increase or decrease the activity of a pathway has driven the accumulation of cis-regulatory variants that act in the same direction on gene expression. Application of this test revealed a variety of yeast pathways with evidence for directional regulatory evolution. In parallel, we also used population genomic sequencing data to compare protein and cis-regulatory variation within and between species. We identified pathways with evidence for divergence within S. cerevisiae, and we detected signatures of positive selection between S. cerevisiae and S. bayanus. Our results point to polygenic, pathway-level change as a common evolutionary mechanism among yeasts. We suggest that pathway analyses, including our test for directional regulatory evolution, will prove to be a relevant and powerful strategy in many evolutionary genomic applications.
gene regulation adaptation yeast
Footnotes
1To whom correspondence should be addressed. E-mail:rbrem@berkeley.edu.
Author contributions: R.B.B. designed research; R.B.B., J.H.B., and Y.M. performed research; J.H.B. and S.D. contributed new reagents/analytic tools; J.H.B., Y.M., S.D., and R.B.B. analyzed data; and J.H.B., S.D., and R.B.B. wrote the paper.
↵*This Direct Submission article had a prearranged editor.
The authors declare no conflict of interest.
Data deposition: GEO data set GSE19837.
This article contains supporting information online at www.pnas.org/cgi/content/full/0912959107/DCSupplemental.
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