Loci, genes, and gene networks associated with life history variation in a model ecological organism,Daphnia pulex(complex)

ABSTRACT Background Identifying the molecular basis of heritable variation provides insight into the underlying mechanisms generating phenotypic variation and the evolutionary history of organismal traits. Life history trait variation is of central importance to ecological and evolutionary dynamics, and contemporary genomic tools permit studies of the basis of this variation in non-genetic model organisms. We used high density genotyping, RNA-Seq gene expression assays, and detailed phenotyping of fourteen ecologically important life history traits in a wild-caught panel of 32 Daphnia pulex clones to explore the molecular basis of trait variation in a model ecological species. Results We found extensive phenotypic and a range of heritable genetic variation (~0 < H 2 < 0.44) in the panel, and accordingly identify 75-261 genes—organized in 3-6 coexpression modules—associated with genetic variation in each trait. The trait-related coexpression modules possess well-supported promoter motifs, and in conjunction with marker variation at trans- loci, suggest a relatively small number of important expression regulators. We further identify a candidate genetic network with SNPs in eight known transcriptional regulators, and dozens of differentially expressed genes, associated with life history variation. The gene-trait associations include numerous un-annotated genes, but also support several a priori hypotheses, including an ecdysone-induced protein and several Gene Ontology pathways. Conclusion The genetic and gene expression architecture of Daphnia life history traits is complex, and our results provide numerous candidate loci, genes, and coexpression modules to be tested as the molecular mechanisms that underlie Daphnia eco-evolutionary dynamics.