The Once and Future Fish: 1300 years of Atlantic herring population structure and demography revealed through ancient DNA and mixed-stock analysis

Atlantic herring populations have been the target of highly profitable coastal and pelagic fisheries in northern Europe for well over a thousand years. Their complex and intermingled population dynamics have sparked extensive debate over the impacts of historical overfishing and have complicated their sustainable management today. Recently developed tools – including diagnostic SNP panels for mixed-stock analysis – aim to improve population assignment for fisheries management, however, the biological relevance of such tools over long periods of time remains unknown. Here, we demonstrate the millennium-long applicability of diagnostic SNP panels and identify population perturbations associated with increasing exploitation pressure and climate change by analyzing whole genome data from modern and ancient herring specimens. We find that herring demographic cycles were likely within healthy ecosystem boundaries until the dramatic disruption of these cycles in the 20th century. We find only autumn-spawning herring in our archaeological remains spanning 900 years from 8 sites across Europe, supporting observations that the numerical dominance of specific spawning populations can demographically outcompete other herring types. We also obtain pre-archival aDNA evidence for the famous, cyclical “Bohuslän periods,” during which mass quantities of North Sea autumn-spawning herring congregated in the Skagerrak. Finally, the long-term applicability of diagnostic SNP panels underscores their highly cost-effective application for the genetic monitoring of herring stocks. Our results highlight the utility of ancient DNA and genomic analysis to obtain historical and natural insights in herring ecology and population dynamics with relevance for sustainable fisheries management.