Disruption of gene expression in hybrids of the fire ants Solenopsis invicta and S. richteri

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

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/8/2012
Publication Date: 3/30/2012
Citation: Ometto, L., Ross, K.G., Shoemaker, D.D., Keller, L. 2012. Disruption of gene expression in hybrids of the fire ants Solenopsis invicta and S. richteri. Molecular Ecology. 21:2488-2501.

Interpretive Summary: Fire ants are considered significant ecological, agricultural, and public health pest throughout their invasive range in the U.S.A. A research entomologist at the Center for Medical, Agricultural, and Veterinary Entomology, USDA-ARS, Gainesville, Florida, a professor and researcher from University of Georgia, a professor and researcher from University of Lausanne, and a scientist from Fondazione Edmund Mach that previously resided at University of Lausanne describe here the results of a study examining levels of gene expression in each of the three castes in North American populations of two introduced fire ants and in their hybrids. The results of this study indicated that only modest hybrid incompatibilities in gene expression exist between the two species. Nonetheless, significant heterogeneity in the degree of hybrid incompatibilities occurs across life stages and castes, suggesting each caste may contribute differently to the divergence and maintenance of separated species in these ants.

Technical Abstract: Transcriptome analyses are a very powerful tool to unveil the distribution and magnitude of genetic incompatibilities in hybridizing taxa. The degree of such hybrid incompatibilities is closely associated with the evolutionary histories of the parental species, and may differ across tissues and between the sexes. In social insects the presence of three castes (males, queens and workers), which experience divergent selection regimes, may further result in distinct patterns and levels of caste-specific hybrid incompatibilities. To investigate the amount of caste-specific hybrid incompatibilities we analyzed the levels of gene expression in adults and pupae of each of the three castes in North American populations of the fire ants S. invicta and S. richteri and in their hybrids. There was a strong component of developmental stage and caste to gene expression. By contrast, the expression variability was only weakly associated with taxonomic identity, with hybrid scores falling between the two parental species’ scores in both life stages and all castes. There were surprisingly modest hybrid incompatibilities between the two species with only very few genes being differently expressed between the hybrids and either parental species. Consistent with the finding of low divergence in gene expression profiles between hybrids and the parental species, there were low levels of disruption in gene regulation in hybrids with only 16 genes mis-expressed in pupae and 18 in adults. The three castes differed greatly in the number of genes mis-expressed, with the male and worker castes each expressing at least seven times more genes than the queen caste in both life stages. Interestingly, many of the mis-expressed genes have been implicated in behavioral variation in Drosophila melanogaster. Overall, the expression profiles of hybrids in both developmental stages were more similar to those of S. richteri than S. invicta, either because S. richteri trans-regulatory elements are on average dominant to those of S. invicta and/or because there is an overall bias in the genetic composition of the hybrids towards S. richteri. Altogether, the results of this study suggest that selection on each caste may contribute differently to interspecific divergence and the process of speciation in these ants as well as in other social insects.