Cracking the Code of Adaptive Evolution (deCODE)

Study systems are needed to definitively test and identify the mechanisms of adaptation to environmental change. Few animal models exist that enable surveys of their natural populations over hundreds or thousands of generations, which are needed to observe genetic fixation of adaptive responses. The extent to which epigenetic adaption precedes and informs genetic fixation is also unknown. Direct measurements of the rates of genetic and epigenetic evolution and associated fitness gains during an adaptation event will lead to improved understanding of the molecular targets of natural selection. We aim to develop and exploit a massively multi-generational system where we can study the process of adaptation on scales ranging from molecules to phenotypes. Our purpose is to radically transform our understanding of how organisms and their populations cope with increasing stresses on ecosystems, by focusing biology's most modern tools towards discovering the molecular targets of natural selection and their contributions to the process of adaptation by phenotypic plasticity, epigenetics and conventional evolution. This knowledge will help policy makers and industry to refine their assessments of environmental health risks and prioritize actions that safeguard biodiversity and vital ecosystem services. In scope with this NERC's call for "research that integrates ecological and evolutionary genetics", we will study the process of adaptation using a premier model species (Daphnia). Arguably, more is known about Daphnia's ecology than all other studied animals. They are keystone species in the food webs of aquatic ecosystems and early indicators of threats to ecosystem health and services. A large research community has established their importance as a model for ecological, toxicological and evolutionary research. We propose to combine field and laboratory experiments to directly observe the processes of acclimation in physiological time scales (plasticity), with natural history experiments to directly observe genetic adaptation through evolutionary time (conventional evolution). Unique discoveries will be made because of Daphnia's parthenogenetic life cycle which alternates clonal and sexual reproduction. This allows for partitioning of phenotypic differences and changes in gene regulation (measured among individuals and populations) into genetic variation, environmental variation and gene-environment interactions for uncovering the molecular genetic and epigenetic basis of phenotypic plasticity. Few other model species produce dormant embryos as part of their life cycle, thereby archiving centuries of population genetic changes within dated lake sediments. We will "resurrect" 100 Daphnia magna from a lake spanning 10 years of adaptation to hypereutrophication, then compete populations from periods that predate human interference to their more modern and adapted decedents. We will associate changes in their genomes, transcriptomes, epigenomes and metabolomes to the documented evolution of fitness related traits. Here we propose to uncover the regulatory pathways for the various modes of adaptation and directly test for a mechanistic link between phenotypic plasticity and the evolution of genetically fixed adaptive traits. We will also infer the genetic basis for the regulatory pathways by discovering the quantitative trait loci that control variation in global mRNA and metabolic profiles for Daphnia including abundance and variance of expression. The segregating levels of variation at these loci will presumably reflect the capacity for populations to adapt and will provide a model to be validated by genome engineering. Finally, we will advance the area of genome engineering (CRISPR) for research on the environment by experiments that will lead to predictive models of the limits of adaption in an ecologically essential species, and more generally, in metazoans that critically support the food chain of inland water ecosystems.