Millennia-Old Coral Holobiont DNA Provides Insight into Future Adaptive Trajectories

Ancient DNA (aDNA) has been applied to evolutionary questions across a wide variety of taxa. Here, we leverage aDNA from millennia-old coral fossil fragments for the first time to gain holistic insights into a rapidly declining western Atlantic reef ecosystem. We sampled four Acropora palmata fragments (dated 4215 BCE - 1099 CE) obtained from two Florida Keys reef cores. From these samples, we established it is possible to both sequence ancient DNA (aDNA) from reef cores and place the data in the context of modern-day genetic variation. We recovered varying amounts of nuclear DNA exhibiting the characteristic signatures of aDNA from all A. palmata fragments. To describe the holobiont sensu lato, which plays a crucial role in reef health, we utilized metagenome-assembled genomes as a reference to recover a large additional proportion of ancient microbial DNA from the samples. The samples shared many common microbes with modern-day coral holobionts from the same reef, suggesting remarkable holobiont stability over time. Comparing the ancient Acropora palmata data to whole-genome sequencing data from living acroporids, we found that while slightly separate, ancient samples were most closely related to individuals of their own species. Together, these results paint a broad picture of coral holobiont change over time and lay a foundation to study historical environmental stress and evolutionary constraints. By better understanding the past genetic pressures on coral, we can gain valuable insights into the adaptive potential and trajectories of reefs under changing climatic conditions in the future.