Hepatic gene expression in herbivores on diets with natural and novel plant secondary compounds

Herbivores are predicted to evolve appropriate mechanisms to process the plant secondary compounds (PSCs) in their diet, and these mechanisms are likely specific to particular suites of PSCs. Changes in diet composition over evolutionary time should select for appropriate alterations in metabolism of the more recent dietary components. We investigated differences in gene expression profiles in the liver with respect to prior ecological and evolutionary experience with PSCs in the desert woodrat, Neotoma lepida. This woodrat species has populations in the Mojave Desert that have switched from feeding on juniper to feeding on creosote at the end of the Holocene as well as populations in the Great Basin Desert that still feed on the ancestral diet of juniper and are naïve to creosote. Juniper and creosote have notable differences in secondary chemistry. Woodrats from the Mojave and Great Basin Deserts were subjected to a fully crossed feeding trial on diets of juniper and creosote after which their livers were analyzed for gene expression. Hybridization of hepatic mRNAs to laboratory rat microarrays resulted in a total of 20,031 genes that met quality control standards. We analyzed differences in large-scale patterns of liver gene expression with respect to GO term enrichment. Diet had a larger effect on gene expression than population membership. However, woodrats with no prior evolutionary experience to the diet upregulated a greater proportion of genes indicative of physiological stress compared with those on their natural diet. This pattern may be the result of a naïve animal's attempting to mitigate physiological damage caused by novel PSCs.