Molecular variation at a candidate gene implicated in the regulation of fire ant social behavior.

Authors: GOTZEK, DIETRICH - UNIVER. OF GEORGIA; Shoemaker, David; ROSS, KENNETH - UNIVER. OF GEORGIA

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/5/2007
Publication Date: 11/8/2007
Citation: Gotzek, D., Shoemaker, D.D., Ross, K.G. 2007. Molecular variation at a candidate gene implicated in the regulation of fire ant social behavior. PLoS One.2(11):1-16.

Interpretive Summary: Fire ants are considered significant ecological, agricultural, and public health pest throughout their invasive range in the U.S.A. Fire ant colonies are headed either by a single reproductive queen (monogyne form) or by multiple queens (polygyne form). This variation in colony social organization also is associated with variation at the single gene Gp-9. A scientist at the Center for Medical, Agricultural, and Veterinary Entomology, USDA, ARS, Gainesville, Florida and scientists from the University of Georgia describe here the results of a study examining Gp-9 evolution in native populations of the red imported fire ant. The discovery of several unique sequences allowed us to confirm the invariant link between the presence of a class of variant alleles and expression of polygyny. Also, our discovery of new alleles allows us to conclude that no single amino acid residue within this gene is completely predictive of polygyne behavior and, thus, potentially causally involved in its expression. This information from such variant colonies is expected to aid progress in connecting the genetic and phenotypic variation underlying regulation of fire ant social behavior and has important implications for biologically-based control methods of fire ants. This study has yielded information of use in bridging functional and population genetic approaches to understanding the genetic basis of an important social trait.

Technical Abstract: The fire ant Solenopsis invicta and its close relatives display a profound social polymorphism involving differences in colony queen number. Colonies are headed by either a single reproductive queen (monogyne form) or multiple queens (polygyne form). This variation in social organization is associated with variation at the gene Gp-9, with monogyne colonies harboring only B-like allelic variants and polygyne colonies always containing b-like variants. We describe naturally occurring variation at Gp-9 in fire ants based on 185 full-length sequences, 136 of which were obtained from S. invicta collected over much of its native range. While there is little overall genetic variation between most of the observed alleles, a surprising amount is found in the coding regions of the gene, with such substitutions usually causing amino acid replacements. This elevated coding-region variation may result from a lack of negative selection acting to constrain amino acid replacements over much of the protein, different rates of mutation accumulation in coding and non-coding sequences, negative selection acting with greater strength on non-coding than coding regions, and/or diversifying selection acting on the protein. Formal selection analyses provide evidence that the latter force played an important role in the basal lineages of the b-like allele clade coincident with the evolution of polygyny. While our data set reveals considerable paraphyly and polyphyly of S. invicta sequences with respect to those of other fire ant species, monophyly of the b-like allele clade was recovered. An expanded analysis of colonies containing alleles of this clade confirmed the invariant link between their presence and expression of polygyny. Finally, our discovery of several unique alleles bearing various combinations of b-like and B-like codons allows us to conclude that no single b-like residue is completely predictive of polygyne behavior and, thus, potentially causally involved in its expression. Rather, all three typical b-like residues appear to be necessary.