The Role of Gene Expression in Task Regulation of the Worker Caste of the Red Imported Fire Ant (Solenopsis Invicta, Buren)

The reproductive ground plan hypothesis suggests that the evolution of social insects has resulted in genes being co-opted from reproductive functions into functions that enable the division of labor. To test this hypothesis in Solenopsis Invicta, I investigated expression of candidate genes important in colony organization. Transcriptome analysis of the worker brains showed no significant differences between carbohydrate and protein foragers, 194 differentially expressed genes were identified between workers in the presence or absence of brood. Among these, two vitellogenin (Vg) genes were identified. S. invicta genome harbors four distinct Vg genes, Vg1, Vg2, Vg3 and Vg4, and both Vg2 and Vg3 were up-regulated in the brains of workers in the absence of brood. In the head, Vg2 and Vg3 were up-regulated in all morphological subcastes in the absence of brood, except for Vg3 in minors and Vgs expression was higher in heads of nurses compared to foragers from colonies with brood. Further, Vg2 was up-regulated in the head of workers in protein-starved colonies. In the whole body, expression analysis of the four Vg genes in workers while in the presence or absence of brood revealed no difference but differences were identified among the morphological subcastes (major workers had higher levels of Vg1 and Vg2). Expression of Vg1 was also higher in carbohydrate foragers when compared to nurses and protein foragers. A phylogenetic analysis of S. invicta hexamerins determined that each of the four predicted proteins clustered with one of the orthologous Apis mellifera hexamerins. Expression analyses revealed queens and nurses had significantly higher expression of all genes compared to the foragers. Hexamerin 1 was expressed at higher level in queens, while hexamerin 2 and arylphorin subunit beta-like were expressed at significantly higher level in nurses. The relationship between the hexamerins and Vgs, and S-hydroprene, a juvenile hormone analog revealed Hexamerin 1 and arylphorin subunit alpha-like expression were significantly lower after application in queens. Hexamerin 2 and arylphorin subunit beta-like expression were significantly lower after application in foragers, and all hexamerins were significantly lower after application in nurses. No effect was seen in the expression of Vg in workers. We have found several differences between A. mellifera and S. invicta, which show that some biological processes which regulate social behavior and colony structure are not conserved between social hymenopterans. These results, the structure of S. invicta colonies (polygyne versus monogyne colonies), and the complete sterility of workers enables future research into unique elements of eusociality which are not able to be observed in A. mellifera and may provide a foundation for the use of S. invicta as a model system to study eusociality in insects