Identification of genetic changes that allow a species to adapt to different environmental conditions is an important topic in evolutionary biology. In this study we analyzed whole-genome resequencing data of Atlantic herring populations from both sides of the Atlantic Ocean and identified a number of loci that show consistent associations with spawning time (spring or autumn). Several of these loci, such as thyroid-stimulating hormone receptor (TSHR), have a well-established role in reproductive biology, whereas others have never been implicated in controlling reproduction. 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.

Abstract

Atlantic herring is an excellent species for studying the genetic basis of adaptation in geographically distant populations because of its characteristically large population sizes and low genetic drift. In this study we compared whole-genome resequencing data of Atlantic herring populations from both sides of the Atlantic Ocean. An important finding was the very low degree of genetic differentiation among geographically distant populations (fixation index = 0.026), suggesting lack of reproductive isolation across the ocean. This feature of the Atlantic herring facilitates the detection of genetic factors affecting adaptation because of the sharp contrast between loci showing genetic differentiation resulting from natural selection and the low background noise resulting from genetic drift. We show that genetic factors associated with timing of reproduction are shared between genetically distinct and geographically distant populations. The genes for thyroid-stimulating hormone receptor (TSHR), the SOX11 transcription factor (SOX11), calmodulin (CALM), and estrogen receptor 2 (ESR2A), all with a significant role in reproductive biology, were among the loci that showed the most consistent association with spawning time throughout the species range. In fact, the same two SNPs located at the 5′ end of TSHR showed the most significant association with spawning time in both the east and west Atlantic. We also identified unexpected haplotype sharing between spring-spawning oceanic herring and autumn-spawning populations across the Atlantic Ocean and the Baltic Sea. The genomic regions showing this pattern are unlikely to control spawning time but may be involved in adaptation to ecological factor(s) shared among these populations.