LAUSR

Significance Ecological disruption due to human impacts is evident worldwide, and a key to mitigation lies in characterizing the underlying mechanisms of species and ecosystem stability. Here we show that three extensive “supergenes” are maintained in Atlantic cod by stabilizing selection, tying these genes to the persistence of a keystone species distributed across the northern Atlantic Ocean. Removal of this species has caused severe ecosystem reshuffling in several areas of its range. Genomic inference of historic stock sizes further shows that cod has been under pressure in the North Sea system since the Viking period, in line with zooarchaeological records. Expansion of fisheries in Northern Europe through the past millennium is well documented and supports the inferred long-term declines. Life on Earth has been characterized by recurring cycles of ecological stasis and disruption, relating biological eras to geological and climatic transitions through the history of our planet. Due to the increasing degree of ecological abruption caused by human influences many advocate that we now have entered the geological era of the Anthropocene, or “the age of man.” Considering the ongoing mass extinction and ecosystem reshuffling observed worldwide, a better understanding of the drivers of ecological stasis will be a requisite for identifying routes of intervention and mitigation. Ecosystem stability may rely on one or a few keystone species, and the loss of such species could potentially have detrimental effects. The Atlantic cod (Gadus morhua) has historically been highly abundant and is considered a keystone species in ecosystems of the northern Atlantic Ocean. Collapses of cod stocks have been observed on both sides of the Atlantic and reported to have detrimental effects that include vast ecosystem reshuffling. By whole-genome resequencing we demonstrate that stabilizing selection maintains three extensive “supergenes” in Atlantic cod, linking these genes to species persistence and ecological stasis. Genomic inference of historic effective population sizes shows continued declines for cod in the North Sea–Skagerrak–Kattegat system through the past millennia, consistent with an early onset of the marine Anthropocene through industrialization and commercialization of fisheries throughout the medieval period.