Environmental PALEO-genomics: using dormant propagules to FORECAST how natural populations can adapt to environmental change

Predicting how evolution shapes the genetic structures of populations has principally relied on investigations through space, in lieu of time, because long-term phenotypic and molecular data are scarce. However, spatial analyses are often limited to a single snapshot in time, that provides inaccurate predictions of changes through time. A temporal perspective is crucial to produce insights into the dynamics and processes, and thus to aid better predictions of adaptive responses to future environmental challenges.
Dormant propagules in sediments, soils and permafrost are convenient natural archives of population-histories from which to trace adaptive trajectories along extended time periods. The water flea Daphnia is a renowned ecological model system that produces dormant egg banks which accumulate to form biological archives. Capitalizing on this system we identify selective and demographic processes driving present-day population genetic structure by analyzing dormant eggs in space and time. We provide solid evidence of differential selection at the genome level under well-characterized environmental gradients in populations distributed at regional scale and identify candidate genes linked to three environmental stressors. We validate these spatial patterns in "time" on populations hatched from biological archives with known history for the same three stressors and in experimental evolution trials. We study how the complex mosaic of biotic and abiotic variables naturally occurring in the landscape contributes to driving neutral and adaptive genetic variation by disentangling the relative role of demographic and adaptive processes.
We conclude that selection plays a major role in determining the population genomic structure of D. magna. Environmental selection directly impacts genetic variation at loci hitchhiking with genes under selection. In addition, priority effects enhanced by local genetic adaptation (cf. monopolization) affect neutral genetic variation by reducing gene flow among populations and genetic diversity within populations.
The temporal perspective offered by the study of biological archives will enhance our ability to predict evolutionary dynamics of natural systems in response to environmental challenges with unprecedented resolution.