Simulated climate change magnifies genetic vulnerabilities from mutation load and maladaptation

As climate change intensifies, the genetic diversity and composition of natural populations will become critical for adaptation and survival. Standing genetic diversity within populations differs across a species range, due to past demographic and natural selection processes driving the accumulation of adaptive, neutral, and deleterious variation. While accumulating genomic knowledge could be used to evaluate population extinction risk from local mal-adaptive genetic makeups, testing such approaches in natural environments remains challenging. Leveraging the genomic resources of Arabidopsis thaliana, we created experimental synthetic populations of similar genetic diversity but differing genetic makeups by mixing 245 natural accessions with different levels of potentially-climate-adaptive alleles and/or genomic burden of deleterious mutations. We planted our populations in a climate change field experiment simulating a gradient of declining rainfall. By tracking survival and reproduction of 135 synthetic experimental populations over three years, we show substantial predictability of genetic makeup on survival and population growth rate. Further, the accumulation of deleterious mutations and locally (mal)adaptive alleles synergistically reduces fitness in increasingly stressful climates. Our findings underscore that for populations to have the greatest chance of surviving climate change, the optimal combination of genomic makeups is essential.