Evolution at two levels in fire ants: the relationship between gene expression and protein evolution

Variation in protein sequence and gene expression each contribute to phenotypic diversity, and thus may be subject to similar selective pressures. Ants and other eusocial insects are particularly useful for investigating the evolutionary link between protein sequence and gene expression because expression variation plays a central role in determining differences between their sexes and castes. We investigated the relationship between protein sequence evolution and gene expression evolution in the fire ants Solenopsis invicta, S. richteri, and their hybrids in order to gain a greater understanding of how selection jointly operates on expression patterns and coding sequence. We found that genes with high expression variability within castes and sexes were frequently differentially expressed between castes and sexes, as well as between species and hybrids. These data indicate that genes showing high variation in expression in one context tend to show high variation in expression in other contexts as well. Our analyses further revealed that gene expression variability in Solenopsis, arising in multiple contexts, was positively associated with rate of protein sequence evolution. These results indicate that gene expression variability is negatively associated with the strength of selective constraint operating on a protein. Overall, our study provides one of the strongest demonstrations that selective constraint mediates both protein sequence evolution and gene expression variability across different biological contexts and timescales.