Genomic insights into diversification and ecological speciation of three Saccharina species

Aim: Saccharina is a genus within the brown algae that is of ecological and economic importance and shows rapid adaptive radiation, while the process and genetic mechanism of diversification and speciation remains unclear. In this study, we conducted genome resequencing of three typical Saccharina species, including the four varieties of S. japonica, and its two sister species (S. angustata and S. longissima) to investigate the genetic mechanism of ecological speciation. Location: coast of Japan Methods: We assess the genomic differentiation and genetic diversity of these Saccharina kelps based on whole-genome resequencing. We applied composite-likelihood approach to identify the ancestral species and reconstruct the evolutionary history. Selective sweep analysis was conducted to detect selective signatures when they adapted to diverse habitat. Results: The demography suggested that S. angustata, S. longissima and S. japonica var. japonica underwent adaptive speciation early, with S. japonica var. japonica as the oldest variant that diverged into three other varieties. The newly evolved variety SR has the highest genetic diversity, and the variety SD has the lowest genetic diversity. Interspecific hybridization among these congeneric species was low, indicating these species exist in genetic isolation in nature. We detected that some stress response genes (e.g. ubiquitin-like protein) and growth-related genes (e.g. imm upregulated 3) were under positive selection during the ecological speciation. Low linkage disequilibrium decay rate and extensive signals of selective sweeps are present in these Saccharina species, providing strong support for adaptive differentiation under natural selection as the driving force for its ecological speciation. Main conclusions: The main driving force of speciation in this genus appears to be not natural hybridization, but genetic isolation and adaptive differentiation by nature selection. The evolutionary history and ecological speciation of Saccharina species allow us to predict how common the species responds to environmental change, and whether they require different management strategies.Funding provided by: National Natural Science Foundation of ChinaCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001809Award Number: 32270389Funding provided by: Chinese Academy of SciencesCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100002367Award Number: 133137KYSB20210034Funding provided by: National Natural Science Foundation of ChinaCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001809Award Number: 3190027