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Published online on November 14, 2007, 10.1073/pnas.0705441104
PNAS | November 20, 2007 | vol. 104 | no. 47 | 18577-18582


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BIOLOGICAL SCIENCES / EVOLUTION
Simpler mode of inheritance of transcriptional variation in male Drosophila melanogaster

Marta L. Wayne*,{dagger},{ddagger}, Marina Telonis-Scott*, Lisa M. Bono§, Larry Harshman, Artyom Kopp||, Sergey V. Nuzhdin**, and Lauren M. McIntyre{dagger},{dagger}{dagger},{ddagger}{ddagger}

*Department of Zoology, University of Florida, Gainesville, FL 32611-8525; {dagger}University of Florida Genetics Institute, University of Florida, Gainesville, FL 32610-3610; §Department of Biological Sciences, Ohio University, Athens, OH 45701-2979; Department of Biological Science, University of Nebraska, Lincoln, NE 68588; ||Department of Evolution and Ecology, University of California, Davis, CA 95616; **Department of Molecular and Computational Biology, University of Southern California, Los Angeles, CA 90089; {dagger}{dagger}Department of Molecular Genetics and Microbiology, University of Florida, Gainesville, FL 32610-0266; and {ddagger}{ddagger}Department of Statistics, University of Florida, Gainesville, FL 32611-8545

Edited by Thomas W. Cline, University of California, Berkeley, CA, and approved September 25, 2007 (received for review June 11, 2007)

Sexual selection drives faster evolution in males. The X chromosome is potentially an important target for sexual selection, because hemizygosity in males permits accumulation of alleles, causing tradeoffs in fitness between sexes. Hemizygosity of the X could cause fundamentally different modes of inheritance between the sexes, with more additive variation in males and more nonadditive variation in females. Indeed, we find that genetic variation for the transcriptome is primarily additive in males but nonadditive in females. As expected, these differences are more pronounced on the X chromosome than the autosomes, but autosomal loci are also affected, possibly because of X-linked transcription factors. These differences may be of evolutionary significance because additive variation responds quickly to selection, whereas nonadditive genetic variation does not. Thus, hemizygosity of the X may underlie much of the faster male evolution of the transcriptome and potentially other phenotypes. Consistent with this prediction, genes that are additive in males and nonadditive in females are overrepresented among genes responding to selection for increased mating speed.

microarray | sexual antagonism | sexual conflict | sexual selection | transcription


Author contributions: M.L.W., L.H., A.K., S.V.N., and L.M.M. designed research; M.L.W. and M.T.-S. performed research; L.M.B. and L.M.M. analyzed data; and M.L.W., L.H., A.K., S.V.N., and L.M.M. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, www.ncbi.nlm.nih.gov/geo (accession nos. GSE5181GSE5183, GSE5189, and GSE5190).

This article contains supporting information online at www.pnas.org/cgi/content/full/0705441104/DC1.

{ddagger}To whom correspondence should be addressed. E-mail: mlwayne{at}zoo.ufl.edu

© 2007 by The National Academy of Sciences of the USA


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