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MBE Advance Access originally published online on July 20, 2005
Molecular Biology and Evolution 2005 22(11):2243-2256; doi:10.1093/molbev/msi219
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© The Author 2005. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oupjournals.org

Research Article

Lineage-Specific Differences in Evolutionary Mode in a Salamander Courtship Pheromone

Catherine A. Palmer*, Richard A. Watts*, Ron G. Gregg{dagger}, Maureen A. McCall{ddagger}, Lynne D. Houck*, Richard Highton§ and Stevan J. Arnold*

* Department of Zoology, Oregon State University; {dagger} Department of Biochemistry and Molecular Biology, School of Medicine, University of Louisville; {ddagger} Department of Psychological and Brain Sciences, University of Louisville; and § Department of Biology, University of Maryland

E-mail: palmerc{at}science.oregonstate.edu.

Functionally equivalent genes may evolve heterogeneously across closely related taxa as a consequence of lineage-specific selective pressures. Such disparate evolutionary modes are especially prevalent in genes that encode postcopulatory reproductive proteins, presumably as a result of sexual selection. We might therefore expect genes that mediate reproduction prior to insemination to evolve in a similar manner. Plethodontid receptivity factor (PRF), a proteinaceous salamander pheromone produced by the male, increases female receptivity during courtship interactions. To test for lineage-specific differences in PRF's evolution, we intensively sampled PRF genes across the eastern Plethodon phylogeny (27 spp.; 34 populations) to compare gene diversification, rates of evolution, modes of selection, and types of amino acid substitution. Our analyses indicate that PRF evolutionary dynamics vary considerably from lineage to lineage. Underlying this heterogeneity, however, are two well-defined transitions in evolutionary mode. The first mode is representative of a typical protein profile, wherein neutral divergence and purifying selection are the dominant features. The second mode is characterized by incessant, cyclical evolution driven by positive selection. In this mode, the positively selected sites are bound by a limited assortment of acceptable amino acids that appear to evolve independently of other sites, resulting in a tremendous number of unique PRF alleles. Several of these selected sites are implicated in receptor binding. These sites are apparently involved in a molecular tango in which the male signal and female receptors coevolve within a confined molecular space. PRF's lineage-specific evolutionary dynamics, in combination with evidence of a molecular tango, highlight the molecular action of sexual selection on a chemical signal that is used during courtship.

Key Words: positive selection • plethodontid receptivity factor • plethodon • courtship pheromone • sexual selection • cytokine


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