Epigenetic mechanisms underlying transgenerational plasticity (TGP)
Epigenetic diversity of temperate to Arctic stickleback populations
TGP and eco-evolutionary dynamics (EED)
Transgenerational plasticity (TGP: where parents prime offspring to perform better in matching future environments) generated by epigenetic mechanisms such as DNA methylation can provide a temporal buffer for genetic adaptation of populations facing rapid climate change. Ultimately, adaptive potential will determine population persistence and species extinction risk in a warming world, but may also play a key role in feedbacks between ecology and evolution (eco-evolutionary dynamics or EED). Direct links between TGP and EED have not yet been investigated in the marine realm. Here, we use populations of marine threespine stickleback (Gasterosteus aculeatus) to identify epigenetic signatures potentially underlying TGP seen at the phenotypic level (physiology and growth) in response to ocean warming, and to disentangle the relative contributions of genetic and epigenetic change to adaptive potential along a latitudinal gradient from the North Sea to the Arctic. Exploring the role of TGP in EED will enlighten whether epigenetic “pre-programming” via inherited adaptive methylomes can modify species interactions, community dynamics and ecosystem function, adding an evolutionary component to ecosystem function models currently based on ecology alone. The project takes a whole-organism and ecosystem approach, while concurrently dissecting these into phenotypic, genetic and epigenetic components, integrating genomics, physiology, life-history, evolution, ecology, and ecosystem modeling.
Lisa is the main PI of the project, and has spent the last few years working on TGP in response to ocean warming using the stickleback model system. Questions that emerged from that work led to this bigger project, where her team now investigates the role of epigenetic variation in TGP (Alex), large-scale population (epi)genetic diversity (Neal), and the role of TGP in eco-evolutionary dynamics (Carl). Of course, none of the work would be possible without our always-happy technician (Timm).
Alex and Lisa just published their first paper together in a special issue of Frontiers in Marine Science focusing on marine environmental epigenetics. Its a genome survey of epigenetic actors in stickleback, with suggestions for how to use some of them in climate change - adaptation studies, as well as in conservation, aquaculture, and assisted evolution. Check it out here.
What's coming next...
Alex conducted an intensive experiment looking at epigenetic reprogramming during gametogenesis and embryogenesis. For that, he acclimated adult fish for 6 weeks at ambient temperature (17°C), +1.5°C and +4°C climate change scenarios, and measured the relative % methylated DNA in brains and gonads after 2, 4 and 6 weeks acclimation. He then measured DNA methylation levels in eggs, sperm, and every embryonic stage until hatching at each of the three experimental temperatures. He found some really cool results which will be presented at ESEB 2019 in the "Transgenerational plasticity in animals" symposium and the "Workshop on causes and consequences of inclusive inheritance" at the Max Planck Institute, Plön in November 2019.
Definitive evidence for parent-to-offspring transgenerational epigenetic inheritance is rare, but necessary to show its evolutionary implications.
Experiment 1a: induce epigenetic modifications underlying TGP (growth, physiology) in response to +1.5°C and +4°C IPCC climate change scenarios.
Dynamics of DNA methylation during early development in zebrafish and killifish (adapted from Fellous et al 2018).
When epigenetic marks are laid down is a key question, since reprogramming during gametogenesis and embryogenesis can lead to "windows for adaptation".
Experiment 1b Gametogenesis: duration and magnitude of climate change cue necessary to induce epigenetic change during reproductive conditioning
Experiment 1c Embryogenesis: epigenetic reprogramming in mature oocytes and sperm, at fertilisation, and at each embryonic developmental stage under 3 climate scenarios