To b or not to b: A pheromone-binding protein regulates colony social organization in fire ants

Abstract

A major distinction in the social organization of ant societies is the number of reproductive queens that reside in a single colony. The fire ant Solenopsis invicta exists in two distinct social forms, one with colonies headed by a single reproductive queen and the other containing several to hundreds of egg-laying queens. This variation in social organization has been shown to be associated with genotypes at the gene Gp-9. Specifically, single-queen colonies have only the B allelic variant of this gene, whereas multiple-queen colonies always have the b variant as well. Subsequent studies revealed that Gp-9 shares the highest sequence similarity with genes encoding pheromone-binding proteins (PBPs). In other insects, PBPs serve as central molecular components in the process of chemical recognition of conspecifics. Fire ant workers regulate the number of egg-laying queens in a colony by accepting queens that produce appropriate chemical signals and destroying those that do not. The likely role of GP-9 in chemoreception suggests that the essential distinction in colony queen number between the single and multiple-queen form originates from differences in workers' abilities to recognize queens. Other, closely related fire ant species seem to regulate colony social organization in a similar fashion.

Potential cause of lethality of an allele implicated in social evolution in fire ants

“…Alleles of this class, which appear to derive from a single b-like ancestor, differ from all ''B-like'' alleles of these species in the amino acids they encode at three positions; b-like alleles encode a glycine residue at position 42 and isoleucine residues at positions 95 and 139, whereas B-like alleles encode serine, methionine, and valine residues, respectively, at these positions. Remarkably, the b allele of S. invicta is unique among the b-like variants, as well as among all other Gp-9 alleles sequenced to date in Solenopsis, because it encodes a lysine rather than a glutamic acid residue at position 151, a substitution that causes a charge change in the protein product (Krieger andRoss 2002, 2005). It is therefore unclear whether the deleterious effects of allele b in homozygous condition are attributable to the presence of amino acid residues at positions 42, 95, and 139 characteristic of all b-like alleles or, instead, are attributable to the presence of the unique chargealtering residue it encodes at position 151.…”

“…Recent studies have begun to catalog the selective forces acting on Gp-9, the nature of molecular variation at this gene, and the phenotypic effects of this variation (see Krieger 2005). Selection has been implicated as playing an important role in this system based in part on observations of unusual genotype distributions in polygyne queens of introduced S. invicta.…”

“…The b allele of introduced S. invicta is just one member of a class of ''b-like'' alleles that invariably are associated with polygyny in the South American species exhibiting social polymorphism (Krieger andRoss 2002, 2005). Alleles of this class, which appear to derive from a single b-like ancestor, differ from all ''B-like'' alleles of these species in the amino acids they encode at three positions; b-like alleles encode a glycine residue at position 42 and isoleucine residues at positions 95 and 139, whereas B-like alleles encode serine, methionine, and valine residues, respectively, at these positions.…”

“…In the USA, where the species is introduced, two coding region variants occur (designated B and b). Monogyne colonies, which have only a single reproductive queen, contain only the B allele, whereas polygyne colonies, which have multiple reproductive queens, contain both the B and b alleles (Ross 1997;Ross and Keller 1998;Krieger 2005). The complete association of Gp-9 allele b with the expression of polygyny in S. invicta is significant because the two social forms differ in many significant reproductive and life history attributes other than colony queen number (Ross and Keller 1995a); thus, variation at this single gene appears to underlie the expression of major alternative adaptive syndromes.…”

“…It is therefore unclear whether the deleterious effects of allele b in homozygous condition are attributable to the presence of amino acid residues at positions 42, 95, and 139 characteristic of all b-like alleles or, instead, are attributable to the presence of the unique chargealtering residue it encodes at position 151. Recent comparative analyses making use of the solved threedimensional structures of several insect OBPs suggest that the residue at position 151 may play a crucial role in the proper functioning of GP-9 protein as a carrier molecule, by affecting either its ability to bind and release ligands or its ability to form biologically active dimers (Krieger 2005). Thus, a radical substitution at this position, such as occurred in the b allele lineage in S. invicta, might be expected to yield a defective protein that ultimately has lethal or otherwise deleterious effects in homozygotes.…”