Local adaptation in Atlantic herring populations

Atlantic herring is a schooling, pelagic fish species that inhabits both sides of the North Atlantic Ocean and the Baltic Sea. It is one of the most abundant marine species with the number of individuals in a herring school being up to a billion. As the habitat of Atlantic herring ranges throughout Baltic Sea and Atlantic Ocean, it shows remarkable adaptation to environmental variables as, for instance, salinity, temperature, light, feed resources and predators are strikingly different between the Baltic Sea and Atlantic Ocean. This has allowed the formation of distinct populations that are locally adapted to a particular environment. Several herring stocks have been recognized in the past based on their morphological features, life history parameters, spawning locations and spawning time.

We use whole genome population sequencing of Atlantic and Baltic herring to reveal the underlying genetic architecture at an unprecedented detailed resolution for both adaptation to a new niche environment and timing of reproduction. We identify almost 500 independent loci associated with a recent niche expansion from marine (Atlantic Ocean) to brackish waters (Baltic Sea), and more than 100 independent loci showing genetic differentiation between spring- and autumn-spawning populations irrespective of geographic origin. Our results show that both coding and non-coding changes contribute to adaptation. Haplotype blocks, often spanning multiple genes and maintained by selection, are associated with genetic differentiation.

Genetic differences associated with spawning time are expected to involve photoperiodic regulation of reproduction. Interestingly, our strongest genetic signal between populations that spawn either in spring or autumn overlapped TSHR that has central role in the photoperiodic regulation in birds and human. Genetic variants associated with adaptation to spring or autumn spawning are shared to a large extent among populations across the Atlantic Ocean and the Baltic Sea, providing evidence for parallel adaptive evolution.