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Title: Relaxed selection is a precursor to the evolution of phenotypic plasticity

Author
item HUNT, BRENDAN - Georgia Institute Of Technology
item OMETTO, LINO - University Of Lausanne
item WURM, YANNICK - University Of Lausanne
item Shoemaker, David
item KELLER, LAURENT - University Of Lausanne
item SOOJIN, YI - Georgia Institute Of Technology
item GOODISMAN, MICHAEL - Georgia Institute Of Technology

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/30/2011
Publication Date: 9/20/2011
Citation: Hunt, B.G., Ometto, L., Wurm, Y., Shoemaker, D.D., Keller, L., Soojin, Y.V., Goodisman, M.A. 2011. Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proceedings of the National Academy of Sciences. 10:1-6.

Interpretive Summary: Fire ants are considered significant ecological, agricultural, and public health pest throughout their invasive range in the U.S.A. A scientist at the Center for Medical, Agricultural, and Veterinary Entomology, USDA-ARS, Gainesville, Florida and scientists from Georgia Institute of Technology and University of Lausanne describe here the results of a study examining expression patterns and evolutionary rates of genes associated with castes, sexes, and developmental stages in fire ants. Our study demonstrates that genes with relaxed selective constraints have a higher propensity for evolving conditional expression between castes, sexes, or developmental stages, that the rate of molecular evolution is higher for conditionally expressed genes than those with ubiquitous expression, and that relaxed selection appears to precede differential gene expression. These combined results suggest that relaxed selection likely has played an underappreciated role in the evolution of different phenotypic responses of similar genotypes to varying environmental conditions.

Technical Abstract: Phenotypic plasticity represents one of the most important ways that organisms adaptively respond to environmental variation. Alternate phenotypes produced through phenotypic plasiticity generally arise through conditional gene expression, which is predicted to result in relaxed selective constraint. However, ancestral relaxation of selection on genes may also act as a predecessor to the evolution of conditional gene expression. Thus, whether relaxed selection acts primarily as a cause or consequence of conditional gene expression remains unclear. Here we show that genes with diminished selective constraints have a higher propensity for evolving conditional expression associated with phenotypic plasticity. By analyzing gene expression patterns associated with specialized castes, sexes, and developmental stages in the fire ant Solenopsis invicta, we first show that the rate of molecular evolution is higher for conditionally expressed genes than those with ubiquitous expression. Surprisingly, we also find that orthologs of genes with caste-biased expression in either S. invicta or the honeybee Apis mellifera exhibit elevated lineage-specific rates of amino acid substitution in taxa lacking castes. Our results indicate that relaxed selection precedes differential gene expression and plays an underappreciated role in the evolution of phenotypic plasticity.