Current Status of a Model System: The Gene Gp-9 and Its Association with Social Organization in Fire Ants

Dietrich Gotzek,Kenneth G Ross,Ryan L Earley

doi:10.1371/journal.pone.0007713

Abstract

The Gp-9 gene in fire ants represents an important model system for studying the evolution of social organization in insects as well as a rich source of information relevant to other major evolutionary topics. An important feature of this system is that polymorphism in social organization is completely associated with allelic variation at Gp-9, such that single-queen colonies (monogyne form) include only inhabitants bearing B-like alleles while multiple-queen colonies (polygyne form) additionally include inhabitants bearing b-like alleles. A recent study of this system by Leal and Ishida (2008) made two major claims, the validity and significance of which we examine here. After reviewing existing literature, analyzing the methods and results of Leal and Ishida (2008), and generating new data from one of their study sites, we conclude that their claim that polygyny can occur in Solenopsis invicta in the U.S.A. in the absence of expression of the b-like allele Gp-9b is unfounded. Moreover, we argue that available information on insect OBPs (the family of proteins to which GP-9 belongs), on the evolutionary/population genetics of Gp-9, and on pheromonal/behavioral control of fire ant colony queen number fails to support their view that GP-9 plays no role in the chemosensory-mediated communication that underpins regulation of social organization. Our analyses lead us to conclude that there are no new reasons to question the existing consensus view of the Gp-9 system outlined in Gotzek and Ross (2007).

Highlights

The genetic and physiological foundations of insect social behavior increasingly are the subjects of study and, as a result, are becoming understood in ever greater detail [1]
The General protein-9 (Gp-9) system in fire ants has emerged as an important model for studying the genetic basis of social evolution in insects as well as a rich source of information relevant to other evolutionary phenomena
While a great deal has been learned about this system over the past decade, enormous gaps remain in our knowledge of the functional role of GP-9 protein, the biochemical and physiological pathways in which the protein functions, the identity of other genetic and biochemical components of these pathways with which Gp-9 interacts, the pheromones involved in mediating worker regulation of queen number, and the specific behaviors by which this regulation is achieved

Summary

Introduction

The genetic and physiological foundations of insect social behavior increasingly are the subjects of study and, as a result, are becoming understood in ever greater detail [1]. The hemolymph distribution of GP-9 as well as the purported lack of expression of a b-like allelic protein in some polygyne S. invicta colonies led LI08 to conclude that ‘‘...it is highly unlikely that GP-9s are involved in olfactory mediation of social organization of the red imported fire ant.’’ In order to evaluate this very general conclusion, it is helpful to distinguish two separate, but interrelated, levels of explanation for the genetic basis of regulation of fire ant social organization, the specific biochemical and physiological pathways in which GP-9 functions and the manner in which variation in these functions affects production and perception of the stimuli modulating worker behaviors toward queens. This oversight stems at least in part from their apparent reliance on an outdated secondary account of fire ant biology [74], information in which has been superseded by recent authoritative reviews of fire ant social biology [4,6] as well as comprehensive behavioral studies aimed at testing the relative roles of Gp-9 genotype and other factors in the regulation of colony queen number [7,11,12]

Discussion

Findings

Materials and Methods