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.

deCODE is a research initiative that is genuinely motivated and focused on transforming environmental health protection. It is conceived by a newly formed (late 2012) and growing interdisciplinary "environmental genomics" research group at the University of Birmingham that has a purpose to deliver scientific leadership in the areas of environmental policy making, regulation and risk assessment, in the UK and abroad. Our approach is to use modern instruments for measuring structure and functional variation of genomes and metabolism of a superb model species (Daphnia) in evolutionary ecology and toxicology, to purposefully contribute mechanistic knowledge that is required to understand and help reduce uncertainty in managing a global and complex environmental health crisis.
Freshwater ecosystems have been described as the most endangered ecosystems in the world. Anthropogenic activities and pollution over the last two centuries have significantly altered the functioning of aquatic ecosystems and their resilience to change. Decision makers are besieged by a significant gap in knowledge required to take effective regulatory actions that protect natural resources and the lives of UK citizens while also safeguarding the UK economy from over-regulation that impacts people's livelihood. Such a delicate balance can only be reached by decisions that are informed by knowing how adaptive processes are controlled and evolve.

Who will benefit from deCODE (outside of related academics)? Policy and decision makers in the UK and EU will benefit most from the outcome of this research. Europe has taken extraordinary legislative steps to protect its natural resources, including the Water Framework Directive (WFD), which is meant to achieve "good ecological status" for all waters on the continent by a set deadline. Yet unlike the REACH legislation (Registration, Evaluation, Authorisation & Restriction of Chemicals) - which has broadened the types of scientific evidence deemed to be useful for safety assessment and has therefore spurred a renaissance for the field of predictive toxicology now focused on discovering response mechanisms that lead to adversity - hazard assessment for ecosystems is still based on prescribed ecotoxicity testing. A mechanistically based approach is required in order to predict the tipping points at which populations reach their buffering capacity limits at coping with environmental change. We are actively collaborating with scientists at the JRC, Ispra, who are integral to the development of science-based policy for freshwater environmental protection in the UK and Europe. These scientists in the Institute for Environment and Sustainability will directly and significantly benefit from this research. Furthermore we are actively engaged (through existing NERC funding) with UK Environment Agency scientists, who will also benefit.

How will they benefit? Our research is designed to support WFD policy, by choosing to study response mechanisms of adaptation in a required test species for regulation (Daphnia included with an algal and a fish species). Moreover, our entire research project is about connecting signatures of population resilience to an urgent and specific environmental problem - hypereutrophication and the quality of freshwater supporting ecosystem services. Insights obtained from this model system have intrinsic value: freshwater ecosystems costs England and Wales over 220M EUR per year and the EU over 2B EUR per year. Our existing collaborations will enable dialogue and the input of this NERC funded science into both UK (via Environment Agency) and European (via JRC) regulatory science. We will begin to develop a brand new knowledge base and set of tools that will directly inform within immediate time-scales the development of policy and mitigation measures.