Genetic Regulation of Colony Social Organization in Fire Ants: An Integrative Overview

Abstract

Expression of colony social organization in fire ants appears to be under the control of a single Mendelian factor of large effect. Variation in colony queen number in Solenopsis invicta and its relatives is associated with allelic variation at the gene Gp-9, but not with variation at other unlinked genes; workers regulate queen identity and number on the basis of Gp-9 genotypic compatibility. Nongenetic factors, such as prior social experience, queen reproductive status, and local environment, have negligible effects on queen numbers which illustrates the nearly complete penetrance of Gp-9. As predicted, queen number can be manipulated experimentally by altering worker Gp-9 genotype frequencies. The Gp-9 allele lineage associated with polygyny in South American fire ants has been retained across multiple speciation events, which may signal the action of balancing selection to maintain social polymorphism in these species. Moreover, positive selection is implicated in driving the molecular evolution of Gp-9 in association with the origin of polygyny. The identity of the product of Gp-9 as an odorant-binding protein suggests plausible scenarios for its direct involvement in the regulation of queen number via a role in chemical communication. While these and other lines of evidence show that Gp-9 represents a legitimate candidate gene of major effect, studies aimed at determining (i) the biochemical pathways in which GP-9 functions; (ii) the phenotypic effects of molecular variation at Gp-9 and other pathway genes; and (iii) the potential involvement of genes in linkage disequilibrium with Gp-9 are needed to elucidate the genetic architecture underlying social organization in fire ants. Information that reveals the links between molecular variation, individual phenotype, and colony-level behaviors, combined with behavioral models that incorporate details of the chemical communication involved in regulating queen number, will yield a novel integrated view of the evolutionary changes underlying a key social adaptation.

Intraspecific variation in social organization by genetic variation, developmental plasticity, social flexibility or entirely extrinsic factors

“…Genetically determined ARTs that could represent ESS occur in several species of fish [28], lizards [27], in ruffs (Philomachus pugnax) [29] and in the isopod Paracerceis sculpta [30]. In fire ants (Solenopsis invicta), the number of breeding queens per colony is determined by the single gene Gp-9, with one queen (monogynous social organization) when only the B-allele is present, but multiple queens ( polygynous social organization) when the b-allele is present as well [31]. The existence of male ARTs alone might not change the social organization unless females also show ARTs [15], but only in a few species do both sexes show ARTs.…”

Cuticular hydrocarbons as queen adoption cues in the invasive Argentine ant

“…In addition, recognition of phenotypic cues by allele matching (recognition-allele mechanism), may also occur (Keller and Ross, 1998). For example, in fire ants, Gp-9 genotypic compatibility seems to regulate queen identity and number via production of a distinct chemical label and formation of a specific exclusionary template based on the allelic variant possessed by workers and queens (Gotzek and Ross, 2007).…”

A Y-like social chromosome causes alternative colony organization in fire ants

“…The fact that Gp-9 codes for an odorant-binding protein (OBP), coupled with evidence that selection acted to drive the molecular divergence of Gp-9b alleles from the ancestral Gp-9B allele, has led to the suggestion that this gene may have a direct role in regulating social organization by means of chemical communication 7,13 . However, because it is unlikely that an OBP also affects traits as diverse as female size, female fecundity and male spermatogenesis, it has been suggested that Gp-9 might be part of a supergene comprising many genes in tight linkage 10,12,14 . The existence of such clusters of loci facilitating the co-segregation of adaptive variation has been demonstrated in some classical cases of floral types (for example, ref.…”

“…However, because it is unlikely that an OBP also affects traits as diverse as female size, female fecundity and male spermatogenesis, it has been suggested that Gp-9 might be part of a supergene comprising many genes in tight linkage 10,12,14 . The existence of such clusters of loci facilitating the co-segregation of adaptive variation has been demonstrated in some classical cases of floral types (for example, ref.…”