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MBE Advance Access published online on June 29, 2005

Molecular Biology and Evolution, doi:10.1093/molbev/msi203
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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
Accepted June 21, 2005

Research Article

Molecular Evolutionary Analyses of the Odorant-Binding Protein Gene Gp-9 in Fire Ants and Other Solenopsis Species

Michael J. B. Krieger 1* and Kenneth G. Ross 2

1 Center for Physics and Biology, Rockefeller University, New York NY 10021, USA
2 Department of Entomology, University of Georgia, Athens GA 30602, USA

* To whom correspondence should be addressed.
Michael J. B. Krieger, E-mail: krieger{at}rockefeller.edu


   Abstract

The fire ant Solenopsis invicta exists in two social forms, one with colonies headed by a single reproductive queen (monogyne form) and the other with colonies containing multiple queens (polygyne form). This variation in social organization is associated with variation at the gene Gp-9, with monogyne colonies harboring only the B allelic variant and polygyne colonies containing b-like variants as well. We generated new Gp-9 sequences from fifteen Solenopsis species and combined these with previously published sequences to conduct a comprehensive, phylogenetically-based study of the molecular evolution of this important gene. The exon/intron structure and the respective lengths of the five exons of Gp-9 are identical across all species examined, and we detected no evidence for intragenic recombination. These data conform to a previous suggestion that Gp-9 lies in a genomic region with low recombination and they indicate that evolution of the coding region in Solenopsis has involved point substitutions only. Our results confirm a link between the presence of b-like alleles and the expression of polygyny in all South American fire ant species known to possess colonies of both social forms. Moreover, phylogenetic analyses show that b-like alleles comprise a derived clade of Gp-9 sequences within the socially polymorphic species, lending further support to the hypothesis that monogyny preceded polygyny in this group of fire ants. Site-specific maximum likelihood tests identified several amino acids that have experienced positive selection, two of which are adjacent to inferred binding-pocket residues in the GP-9 protein. Four other binding-pocket residues are variable among fire ant species, although selection is not implicated in this variation. Branch-specific tests revealed strong positive selection on the stem lineage of the b-like allele clade, as expected if selection drove the amino acid replacements crucial to the expression of polygyne social organization. Such selection may have operated via the ligand-binding properties of GP-9, as one of the two amino acids uniquely shared by all b-like alleles is predicted to be a binding-pocket residue.

Keywords: fire ants; Gp-9; odorant-binding proteins; polygyny; Solenopsis.
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