Polygenic and monogenic adaptation drive evolutionary rescue at different magnitudes of environmental change

Abstract

Understanding the genetic basis of rapid adaptation is key to predicting species evolutionary responses to environmental change. However, it is still debatable whether many small-effect mutations or a few large-effect mutations underlie rapid adaptation, and how this knowledge can predict population survival or extinction. To address this question, we performed a series of ecologically grounded forward-in-time genetic simulations to study rapid adaptation and extinction with increasing magnitudes of environmental change. These simulations were seeded with genomic variation of the plant Arabidopsis thaliana to have a realistic genomic structure, with one (monogenic) to 1,000 (polygenic) variants with varying heritabilities contributing to an environmental adaptive trait. Our results revealed two distinct scenarios of rapid adaptation and population rescue. Under small to moderate environmental shifts, high polygenic traits increased evolutionary rescue probability. Under extreme environmental shifts, high polygenic traits lead predictably to extinction, yet monogenic traits sometimes produce one-off winning adaptive genotypes. We interpret our rapid evolutionary rescue findings in terms of the fundamental theorem of natural selection, where monogenic and polygenic traits differ in how they create stable versus skewed fitness variance (Vw) and how they respond to environmental shifts. These results highlight the insights genomics gives us into the (un)predictability of species evolutionary responses to global change, with management implications for assisted adaptation conservation.