Evolutionary origin of a novel gene expression pattern through co-option of the latent activities of existing regulatory sequences
Mark Rebeiz a,b,1, Nick Jikomes a,1, Victoria A. Kassner a, and Sean B. Carroll a,2
Author Affiliations
aHoward Hughes Medical Institute and Laboratory of Molecular Biology, University of Wisconsin, Madison, WI 53706; and
bDepartment of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15260
Contributed by Sean B. Carroll, April 20, 2011 (sent for review February 28, 2011)
Abstract
Spatiotemporal changes in gene expression underlie many evolutionary novelties in nature. However, the evolutionary origins of novel expression patterns, and the transcriptional control elements (“enhancers”) that govern them, remain unclear. Here, we sought to explore the molecular genetic mechanisms by which new enhancers arise. We undertook a survey of closely related Drosophila species to identify recently evolved novel gene expression patterns and traced their evolutionary history. Analyses of gene expression in a variety of developing tissues of the Drosophila melanogaster species subgroup revealed high rates of expression pattern divergence, including numerous evolutionary losses, heterochronic shifts, and expansions or contractions of expression domains. However, gains of novel expression patterns were much less frequent. One gain was observed for the Neprilysin-1 (Nep1) gene, which has evolved a unique expression pattern in optic lobe neuroblasts of Drosophila santomea. Dissection of the Nep1 cis-regulatory region localized a newly derived optic lobe enhancer activity to a region of an intron that has accumulated a small number of mutations. The Nep1 optic lobe enhancer overlaps with other enhancer activities, from which the novel activity was co-opted. We suggest that the novel optic lobe enhancer evolved by exploiting the cryptic activity of extant regulatory sequences, and this may reflect a general mechanism whereby new enhancers evolve.
cis regulation, enhancer evolution, gene regulation, novelty
Footnotes
1M.R. and N.J. contributed equally to this work.
2To whom correspondence should be addressed. E-mail:sbcarrol@wisc.edu.
Author contributions: M.R., N.J., and S.B.C. designed research; M.R., N.J., and V.A.K. performed research; M.R. and N.J. analyzed data; and M.R., N.J., and S.B.C. wrote the paper.
This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected in 2007.
The authors declare no conflict of interest.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. JF838123–JF838169).
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