Introduction
One of the fundamental questions in biology is how organisms adapt to
diverse and changing environments (Schluter, 2000). Spatially varying
selection usually triggers differential adaptations of local populations
and ultimately initiates evolutionary diversification and speciation
(Fustier et al., 2017; Ferchaud & Hansen, 2016). Identification of the
genetic basis for ecological adaptation is not only a primary goal in
evolutionary biology, but it is also required to appropriately define
conservation units (CUs) to help guide management and conservation
efforts in changing environments (Chen et al., 2018; Skelly et al.,
2007; Balanya, Huey, Gilchrist, & Serra, 2009). Moreover, detecting
candidate genes under natural selection can help identify the key gene
pathways involved in adaptations to local environments. Marine
environments are dramatically changing, and one of the most influential
changes is rising temperature. Temperature represents a major
environmental factor that influences spatial distribution and diversity
of fish species (Chen, Farrell, Matala, Hoffman, & Narum, 2018).
Advancing our understanding of thermal adaptation is critical in
predicting adaptive potential and ecological consequences of
anthropogenic global warming.
Global climate change has considerable effects on organisms, especially
for coastal species. In particular, the influence of climate change on
marine organisms is reinforced in the East China Sea and the Yellow Sea,
in which the water is warming at a higher rate than in other areas (Cai,
Han, & Yang, 2020). Simulation results showed that even under the low
greenhouse emission scenario (i.e., RCP 4.5), the average annual sea
surface temperature in the Yellow Sea would increase by at least 2 °C by
the end of the 21st century
(http://www.bio-oracle.org/)
(Assis et al., 2018). Therefore, climate-mediated selective signatures
must be detected. Restriction site-associated DNA tags sequencing
(RAD-seq) and genotyping-by-sequencing (GBS) methods have been applied
in investigating the genetic adaptations of organisms in the
Northwestern Pacific. However, these methods only cover a fraction of
the total genome and may miss numerous loci under selection in local
adaptations (Li, Xue, Zhang, & Liu, 2018; Wang et al., 2016; Xu et al.,
2017). Furthermore, the population genomics studies conducted in this
region only revealed a possible signature of thermal adaptation, and no
population-specific genome region or gene-related to warm or cold
temperature has been analyzed. Adaptations to high or cold temperatures
are expected to have a highly polygenic background, which is difficult
to detect using reduced-representation sequencing genome scans. In
addition to possible local adaptations, the similar distribution of
ocean surface temperature between the coastal waters of China and Japan
may lead to identical or similar adaptive changes in distantly
independent populations, thereby causing parallel evolution.
Our recent population-scale genomic study on the Japanese whiting,Sillago japonica (Family Sillaginidae), demonstrated that this
species is an ideal model for detecting signatures of parallel selection
(Kashiwagi, Kondo, Yoshida, & Yoshioka, 2000). This fish is a
commercially important coastal species widely distributed throughout the
Northwestern Pacific, especially in the East China Sea, the Yellow Sea,
and the coastal waters of Japan (McKay, 1992; Oozeki, Hwang, & Hirano,
1992). This species is euryhaline but is not observed to migrate over
long distances (Yang, Gao, Meng, & Jiang, 2020). GBS markers indicated
substantial genetic differentiation between Chinese and Japanese
populations, with Rushan (Weihai City, China) population as the
transition population between China and Japan (Kashiwagi, Kondo,
Yoshida, & Yoshioka, 2000). These findings supported the supposition
that the S. japonica populations in the East China Sea and the
coastal waters of Japan are independent genetic populations. The Yellow
Sea population that disperses from the East China Sea might be able to
tolerate cold temperature stress during winter and induce adaptation to
cold temperature on the genome. The west coast of East China Sea
populations from China and some Japan populations encounter similar
temperature stress that may cause parallel evolution and natural
selection on the same genes. Therefore, S. japonica is an
interesting species for studies of ecological adaptation because it
inhabits diverse environments ranging from tropical to warm temperate
climates, and it has low levels of genetic differentiation at the
neutral loci (Gao, Yang, Yanagimoto, & Xiao, 2019; Kashiwagi, Kondo,
Yoshida, & Yoshioka, 2000). The draft genome of S. japonica has
been completed by the BGI-Shenzhen company (unpublished data). This
draft genome provides a fundamental resource that enables the whole
resequencing of genomes and the conduct of population genomic research.
In the present study, we sequenced the whole genome of 49 S.
japonica individuals collected from five sites across the coastal
waters of China and Japan that cover high-temperature (mean annual
temperature > 25 ℃), warm-temperature (mean annual
temperature > 19℃), and cold-temperature (mean annual
temperature > 14 ℃) areas. This study provides insights
into the evolutionary history and genetic diversity of S.
japonica , as well as an example of mechanisms by which a species can
adapt to regions with different thermal environments. By comparing the
genomes of S. japonica from cold- and high-temperature
environments, we identified candidate genes with molecular functions
that are potentially involved in local adaptations to temperature amongS. japonica inhabiting different thermal environments. The
comparison of S. japonica populations from the East China Sea and
the coastal waters of Japan may provide possible evidence for parallel
evolution within this species.