Evidence of positive polygenic selection following a series of environmental and demographic disasters in Pacific herring

The causes and consequences of population collapse and recovery are difficult to discern and therefore predict because historical data are often sparse, and environmental drivers may interact in complex ways. Yet the influence of environmental change can imprint in contemporary and historic DNA sequences, thereby offering clues about drivers of population dynamics. The Prince William Sound (PWS) stock of Pacific herring famously collapsed in the early 1990s following the Exxon Valdez oil spill (EVOS), yet the causes of the collapse and reasons for a persistent lack of recovery are controversial. Three seasons after the spill, the PWS population declined precipitously, coincident with repeated disease outbreaks, and has remained small across the three decades since. We use population genetics as a forensic tool to gain insight into the causes and consequences of the collapse. We tracked genome-wide genetic variation across time, spanning the period immediately after the spill but preceding the collapse (1991) and across three subsequent decades to 2017. We compared genetic change through time between the PWS population and two reference Alaska populations. We detected high genetic differentiation between the Bering Sea and the Gulf of Alaska, and relatively small but significant genetic structure within the Gulf of Alaska. No loss of genome-wide genetic diversity was observed in the PWS population after the collapse. We did not detect any evidence for selective sweeps at individual loci. However, using sensitive temporal covariance methods, we detected significant signatures of positive polygenic adaptation in the PWS population but not in either of the reference populations. Gene functional enrichment analysis is consistent with selection acting on immune function and pathways that regulate crude oil developmental toxicity in the period following the spill and collapse. This suggests that environmental perturbations unique to the PWS region, including oil spills and disease outbreaks, affected the fitness of resident fish, and shifted their population genetic trajectory.