Background: Saccharina japonica is a commercially and ecologically important seaweed and shows rapid ecological speciation. This kelp represents an excellent model for understanding the process and genetic mechanism of diversification and speciation of brown seaweeds. Up to now, there was limited research about the ecological speciation of seaweeds from a genomic perspective. In this study, we conducted genome resequencing of four varieties of S. japonica and two sister species (S. angustata and S. longissima) to investigate the genetic mechanism of ecological speciation.

Results: The demographic history suggests that the lineage of S. angustata and S. longissima is a sister lineage to that of S. japonica, rather than its direct ancestor, with the genetic lineage of S. japonica var. religiosa diverging earliest from the rest of the taxa. Even though there is lower genetic differentiation among these varieties, natural hybridization and gene flow are limited. We detected some heat resistance (e.g., heat shock protein 70), stress response (e.g., ubiquitin-like protein), and growth-related genes (e.g., immediate upright (imm) upregulated 3) were under positive selection during the ecological speciation. Low linkage disequilibrium decay rate and extensive signals of selective sweeps were detected in these varieties, suggesting that adaptive differentiation under natural selection was the driving force for ecological speciation.

Conclusions: The main force driving speciation in this species does not appear to be ongoing hybridization but historical admixture and adaptive differentiation due to natural selection. An understanding of the evolutionary history and ecological speciation of S. japonica represents an important prerequisite for effective use of germplasm in breeding and for the conservation of natural resources.