Population genomics of resource exploitation: insights from gene expression profiles of two Daphnia ecotypes fed alternate resources

Consumer-resource interactions are a central issue in evolutionary and community ecology because they play important roles in selection and population regulation. Most consumers encounter resource variation at multiple scales, and respond through phenotypic plasticity in the short term or evolutionary divergence in the long term. The key traits for these responses may influence resource acquisition, assimilation, and/or allocation. To identify relevant candidate genes, we experimentally assayed genome-wide gene expression in pond and lake Daphnia ecotypes exposed to alternate resource environments. One was a simple, high-quality laboratory diet, Ankistrodesmus falcatus. The other was the complex natural seston from a large lake. In temporary ponds, Daphnia generally experience high-quality, abundant resources, whereas lakes provide low-quality, seasonally shifting resources that are chronically limiting. For both ecotypes, we used replicate clones drawn from a number of separate populations. Fourteen genes were differentially regulated with respect to resources, including genes involved in gut processes, resource allocation, and activities with no obvious connection to resource exploitation. Three genes were differentially regulated in both ecotypes; the others may play a role in ecological divergence. Genes clearly linked to gut processes include two peritrophic matrix proteins, a Niemann-Pick type C2 gene, and a chymotrypsin. A pancreatic lipase, an epoxide hydrolase, a neuroparsin, and an UDP-dependent glucuronyltransferase are potentially involved in resource allocation through effects on energy processing and storage or hormone pathways. We performed quantitative rt-PCR for eight genes in independent samples of three clones of each of the two ecotypes. Though these largely confirmed observed differential regulation, some genes' expression was highly variable among clones. Our results demonstrate the value of matching the level of biological replication in genome-wide assays to the question, as it gave us insight into ecotype-level responses at ecological and evolutionary scales despite substantial variation within ecotypes.