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.