Evolution of gene expression in fire ants: the effects of developmental stage, caste, and species

Authors: OMETTO, LINO - University Of Lausanne; Shoemaker, David; ROSS, KENNETH - University Of Georgia; KELLER, LAURENT - University Of Lausanne

Submitted to: Molecular Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/20/2010
Publication Date: 12/22/2010
Citation: Ometto, L., Shoemaker, D.D., Ross, K.G., Keller, L. 2010. Evolution of gene expression in fire ants: the effects of developmental stage, caste, and species. Molecular Biology and Evolution. 28:1381-1392.

Interpretive Summary: Fire ants are considered significant ecological, agricultural, and public health pest throughout their invasive range in the U.S.A. A Scientist at the Center for Medical, Agricultural, and Veterinary Entomology, USDA-ARS, Gainesville, Florida and scientists from several institutions around the world describe here the results of a study investigating gene expression patterns in different castes and life stages of two fire ant species to obtain a comprehensive picture of the relative contributions of gender (sex), caste, developmental stage, and species divergence to gene expression evolution. The results of this study suggest much of the evolution of gene expression in fire ants may occur in the worker caste, despite the fact that these individuals are largely or completely sterile. Analyses of gene expression evolution also revealed a combination of positive selection and relaxation of stabilizing selection as important factors driving the evolution of such genes.

Technical Abstract: Ants provide remarkable examples of equivalent genotypes developing into divergent and discrete phenotypes. Diploid eggs can develop either into queens, which specialize in reproduction, or workers, which participate in cooperative tasks such as building the nest, collecting food, and rearing the young. In contrast, the differentiation between males and females generally depends upon whether eggs are fertilized, with fertilized (diploid) eggs giving rise to females and unfertilized (haploid) eggs giving rise to males. To obtain a comprehensive picture of the relative contributions of gender (sex), caste, developmental stage, and species divergence to gene expression evolution, we investigated gene expression patterns in pupal and adult queens, workers, and males of two species of fire ants, Solenopsis invicta and S. richteri. Microarray hybridizations revealed that variation in gene expression profiles is influenced more by developmental stage than by caste membership, sex, or species identity. The second major contributor to variation in gene expression was the combination of sex and caste. Although workers and queens share equivalent diploid nuclear genomes, they have highly distinctive patterns of gene expression in both the pupal and adult stages, as might be expected given their extraordinary level of phenotypic differentiation. Overall, the difference in the proportion of differentially-expressed genes was greater between workers and males than between workers and queens or queens and males, consistent with the fact that workers and males share neither gender nor reproductive capability. Moreover, between-species comparisons revealed that the greatest difference in gene expression patterns occurred in adult workers, a finding consistent with the fact that adult workers most directly experience the distinct external environments characterizing the different habitats occupied by the two species. Thus, much of the evolution of gene expression in ants may occur in the worker caste, despite the fact that these individuals are largely or completely sterile. Analyses of gene expression evolution revealed a combination of positive selection and relaxation of stabilizing selection as important factors driving the evolution of such genes.