Genome-Wide Expression Patterns and the Genetic Architecture of a Fundamental Social Trait

John Wang,Laurent Keller,Kenneth G Ross

doi:10.1371/journal.pgen.1000127

John Wang, Laurent Keller + Show 1 more

Open Access

https://doi.org/10.1371/journal.pgen.1000127

Copy DOI

Journal: PLoS Genetics	Publication Date: Jul 18, 2008
Citations: 130	License type: CC BY 4.0

Affiliation: University of Lausanne, University of Georgia

Abstract

Explaining how interactions between genes and the environment influence social behavior is a fundamental research goal, yet there is limited relevant information for species exhibiting natural variation in social organization. The fire ant Solenopsis invicta is characterized by a remarkable form of social polymorphism, with the presence of one or several queens per colony and the expression of other phenotypic and behavioral differences being completely associated with allelic variation at a single Mendelian factor marked by the gene Gp-9. Microarray analyses of adult workers revealed that differences in the Gp-9 genotype are associated with the differential expression of an unexpectedly small number of genes, many of which have predicted functions, implying a role in chemical communication relevant to the regulation of colony queen number. Even more surprisingly, worker gene expression profiles are more strongly influenced by indirect effects associated with the Gp-9 genotypic composition within their colony than by the direct effect of their own Gp-9 genotype. This constitutes an unusual example of an “extended phenotype” and suggests a complex genetic architecture with a single Mendelian factor, directly and indirectly influencing the individual behaviors that, in aggregate, produce an emergent colony-level phenotype.

Highlights

Considerable interest surrounds the genetic architectures underlying fundamental adaptive traits in wild populations [1,2,3,4,5]
Information on the genetic architecture of social organization is essential to constructing realistic models of social evolution that can answer questions about the numbers and types of genetic changes necessary to change a solitary to a social animal or to convert a simple society to a large and highly complex one [13]
A remarkable case of a fundamental social polymorphism that appears to be under simple genetic control is variation in colony social organization in the fire ant Solenopsis invicta

Summary

Introduction

Considerable interest surrounds the genetic architectures underlying fundamental adaptive traits in wild populations [1,2,3,4,5]. A remarkable case of a fundamental social polymorphism that appears to be under simple genetic control (single Mendelian factor of large effect) is variation in colony social organization in the fire ant Solenopsis invicta In this species a single genomic element marked by the protein-encoding gene Gp-9 is implicated in the production of two distinct types of queens that differ in physiology, fecundity and behavior [14,15,16,17,18,19]. This genetic factor determines whether workers tolerate a single fertile queen (monogyne social form) or multiple queens (polygyne social form) in their colony.

Author Summary

Findings

Materials and Methods