Phylogeographic diversification and postglacial range dynamics shed light on the conservation of the kelp Saccharina japonica.

Jie Zhang,Delin Duan,Chikako Nagasato,Jianting Yao,Tatiana N Krupnova,Zi‐Min Hu,Alexander Jueterbock,Norishige Yotsukura

doi:10.1111/eva.12756

Abstract

Studies of postglacial range shifts could enhance our understanding of seaweed species’ responses to climate change and hence facilitate the conservation of natural resources. However, the distribution dynamics and phylogeographic diversification of the commercially and ecologically important kelp Saccharina japonica in the Northwest Pacific (NWP) are still poorly surveyed. In this study, we analyzed the evolutionary history of S. japonica using two mitochondrial markers and 24 nuclear microsatellites. A STRUCTURE analysis revealed two partially isolated lineages: lineage H, which is scattered along the coast of Japan; and lineage P, which occurs along the west coast of the Japan Sea. Ecological niche modeling projections to the Last Glacial Maximum (LGM) revealed that the southern coasts of the Japan Sea and the Pacific side of the Oshima and Honshu Peninsulas provided the most suitable habitats for S. japonica, implying that these regions served as ancient refugia during the LGM. Ancient isolation in different refugia may explain the observed divergence between lineages P and H. An approximate Bayesian computation analysis indicated that the two lineages experienced post‐LGM range expansion and that postglacial secondary contact occurred in Sakhalin. Model projections into the year 2,100 predicted that S. japonica will shift northwards and lose its genetic diversity center on the Oshima Peninsula in Hokkaido and Shimokita Peninsula in Honshu. The range shifts and evolutionary history of S. japonica improve our understanding of how climate change impacted the distribution range and diversity of this species and provide useful information for the conservation of natural resources under ongoing environmental change in the NWP.

Highlights

Climate changes during the late Pleistocene glaciations influenced the present‐day distribution and phylogeographic structure of ma‐ rine flora and fauna (e.g., Coyer, Peters, Stam, & Olsen, 2003; Hansen, Mensberg, & Berg, 1999; Liu, Gao, Wu, & Zhang, 2007; Reusch, Stam, & Olsen, 2000)
Numerous species worldwide respond to modern climate change with poleward range shifts (Davis & Shaw, 2001; Parmesan & Yohe, 2003; Rosenzweig et al, 2008), and ample evidence has shown that modern climate change reduces the range of seaweeds and leads to decline in natural resources (Assis et al, 2017; Fernandez, 2011; Smale & Wernberg, 2013; Wernberg, Russell, Thomsen et al, 2011)
Bayesian analyses of population structure using concatenated Mitochondrial DNA (mtDNA) sequences detected four genetic clusters: cluster 1 included populations in Hokkaido, Korea, and the east coast of Sakhalin; clus‐ ter 2 was observed only on the northwestern coast of Hokkaido; cluster 3 consisted of populations around Honshu Island; and clus‐ ter 4 contained most of the populations from the west coast of the Japan Sea and the west coast of Sakhalin (Supporting Information Figure S6)

Summary

| INTRODUCTION

Climate changes during the late Pleistocene glaciations influenced the present‐day distribution and phylogeographic structure of ma‐ rine flora and fauna (e.g., Coyer, Peters, Stam, & Olsen, 2003; Hansen, Mensberg, & Berg, 1999; Liu, Gao, Wu, & Zhang, 2007; Reusch, Stam, & Olsen, 2000). Saccharina japonica is a cold‐temperature brown seaweed that is native to northern Japan and Far Eastern Russia (Supporting Information Figure S1), and it was introduced to northern China and South Korea in the early 1920s and 1970s, respectively (Hwang, Ha, & Park, 2018; Tseng & Wu, 1962) This kelp is en‐ demic and dominant in the north of the Japan Sea and provides an ideal model to analyze how the climate changes have influ‐ enced the genetic diversity and postglacial range shifts of kelps in this region. Our objectives were to (a) iden‐ tify potential glacial refugia and subsequent recolonization routes; (b) investigate how the opening of the four straits along the Japan Sea influenced the distribution patterns and secondary contact; and (c) as‐ sess how climate change affected the range shift of S. japonica

| MATERIALS AND METHODS

| DISCUSSION

Findings

| CONCLUSION