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.