New insight on the genetic structure of S. japonica
The historical and present variable environment has profound effects on the genetic variation of species. Analyses at the genomic level provide detailed information about the genetic structure, population history, and adaptation to various environments and facilitate species protection and fishery management (Li, Xue, Zhang, & Liu, 2018). The present population genomic study delineated the fine population genetic characteristics of S. japonica populations via whole-genome sequencing. In the Northwestern Pacific, this study may be the first to adopt whole-genome sequencing in assessing population differentiation and signatures of selection in a marine fish species. Analyses of the population history suggested that the historical sea level has had a substantial influence on the effective population size of species, with a warmer climate facilitating population growth. Several genes related to adaptations to local environments were identified in the present study.
The present study provided a higher resolution of population structure compared with that identified in previous studies based on GBS, mtDNA control region, and morphological data (Gao, Yang, Yanagimoto, & Xiao, 2019; Xue, Du, & Gao, 2010). On the basis of the morphological analysis of S. japonica , Xue et al. found no significant population differentiation among populations from the Yellow Sea, East China Sea, and the South China Sea (Gao, Yang, Yanagimoto, & Xiao, 2019). Researchers have attempted to use the mtDNA control region in finding genetic differentiation in this species. Gao et al. detected no genetic structure in S. japonica owing to the short fragment of this region (Gao, Yang, Yanagimoto, & Xiao, 2019). However, using GBS technology, Yang et al. observed considerable genetic differentiation between the China and Japan populations ofS. japonica (Kashiwagi, Kondo, Yoshida, & Yoshioka, 2000), but they failed to completely separate the individuals from these populations. In contrast to the mtDNA and GBS results of S. japonica , the present study revealed the complete genetic break between the China and Japan populations according to whole-genome sequencing data. PCA further distinguished the three China populations.
Numerous researchers have suggested that Pleistocene glaciations are the most important events that shaped the phylogeographic genetic structures of extant species (Han, Wang, Gao, Yanagimoto, & Lida, 2018). The complete divergence between the China and Japan populations likely reflected historical isolation between the East China Sea and the Pacific Ocean during the Pleistocene low sea-level stands. In the present study, population demographic analysis suggested a divergence time of 30 Ka between the two clades during the last glacial period. The dating of divergence was consistent with geological events that might have created a vicariant barrier between the S. japonicapopulations of the Pacific Ocean and the East China Sea.
Mantel tests identified a strong relationship between coastline distance and genetic differentiation. The ocean distance that separates the western and eastern East China Sea is identified as a physical barrier that restricts gene flow between samples. Considering the life history of this species and the physical environment in the East China Sea, long ocean distance is a reasonable physical barrier for a demersal species. Ocean depth (<30m) limits the distribution of S. japonica in marine waters (FishBase,https://www.fishbase.in/summary/Sillago-japonica.html). The average depth of the East China Sea is about , with a maximum of at the continental slope (Guan, & Mao, 1982). Therefore, the depth of water in the direct dispersal route between the coastal waters of Japan might have formed an unsuitable habitat for this species and prevented its offshore dispersal. The historical migration event from the TB to RS populations and no migration from the Japan populations to the ZS population supported the coastal dispersal pattern. The coastal dispersal pattern was also supported by the potential distribution areas of two groups as predicted by Maxent model. The coastal dispersal pattern was also observed in Japanese grenadier anchovy,Coilia nasus (Gao, Wan, Song, Zhang, & Han, 2014; Han, Han, Wang, & Gao, 2015). C. nasusshares similar biological characteristics and geographic distribution in the East China Sea with S. japonica . AFLP and mtDNA results ofC. nasus confirmed that direct ocean distance with deepwater at the continental slope between the western and eastern coastal waters of the East China Sea served as a major physical barrier to this species.
The different demographic trajectories of the S. japonicapopulations might have resulted from geographic and climatic differences. Moreover, the TB and IB populations showed a slower increase compared with the China populations during the same time. The Japan populations (TB and IB) were mainly distributed in the coastal waters of Japan and thus might have suffered less impact during the Pleistocene glaciations. The expansion of population size in the China and Japan populations was consistent with the historical sea-level rise during the interglacial periods. The population started to increase dramatically about 30 Ka before the present when the Wurm glacial stage began to end in the Northwestern Pacific (Kawahata & Ohshima, 2004).
Previous studies revealed that marine pelagic and demersal fishes in the coastal waters of China are expected to exhibit little intraspecific genetic structuring derived from the ocean currents and the apparent lack of physical barriers (Han, Gao, Yanagimoto, & Sakurai, 2008). Given the wide distribution and ecological characters of S. japonica , this species might be susceptible to a heterogeneous local environment. Likewise, genome-wide SNPs revealed remarkable regional differentiation between northern and southern populations in recent genomic studies of the roughskin sculpin (Trachidermus fasciatus ), the marbled rockfish (Sebastiscus marmoratus ), the spotted seabass (Lateolabrax maculatus ), and the small yellow croaker (Larimichthys polyactis ) (Li, Xue, Zhang, & Liu, 2018; Xu et al., 2017; Liu, Zhang, Xue, Gao, & Liu, 2016). In this sense, the high degree of regional differentiation between the northern and southern Chinese populations might be common in marine fish species owing to local adaptations to a heterogeneous environment. For instance, the average annual sea surface temperature ranges from 15.9 °C in the RS population to 25.2 °C in the ST population (data provided by the Bio-ORACLE). This obvious difference in the thermal environment might have resulted in divergent selection on specific genes. The genetic diversity in certain genome regions would be substantially decreased as a result of natural selection.