Whole-genome resequencing of Japanese whiting (Sillago japonica) provide insights into local adaptations
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摘要: 西北太平洋地区海洋生物对不同环境的适应进化研究尚未系统开展。种群之间的基因组差异能够反映环境选择作用。开展海洋生物群体对温度适应进化研究对于理解生物对气候变化的适应机制以及预测生物对全球变暖的未来适应潜力非常重要。我们采集了少鳞鱚（Sillago japonica）中国和日本近海不同纬度的地理群体样品，利用全基因组重测序检测研究温度适应机制。我们对5个群体基因组重测序，获得548万个单核苷酸多态位点（SNPs），可以将中国和日本群体完全区分开。这种遗传结局形成主要是归因于地理隔离和本地适应性。两个隔离的种群（舟山和伊势湾/东京湾）之间共享大量受选择基因，这表明两种群间存在温度驱动的平行进化现象。这也表明温度对不同种群的选择过程可能是可重复的。此外，我们观察到冷适应的受选择基因在功能上主要跟细胞膜的流动性相关。物种分布预测模型表明，少鳞鱚中国和日本群体可能对未来的气候变化有不同的响应，在未来前者分布区将扩大，后者分布区将收缩。该研究的结果促进了对鱼类群体本地温度适应的遗传机制的理解，扩大了我们对群体遗传分化和群体如何适应温度变化的新认知。Abstract: The genetic adaptations of various organisms to heterogeneous environments in the northwestern Pacific remain poorly understood. Heterogeneous genomic divergence among populations may reflect environmental selection. Advancing our understanding of the mechanisms by which organisms adapt to different temperatures in response to climate change and predicting the adaptive potential and ecological consequences of anthropogenic global warming are critical. We sequenced the whole genomes of Japanese whiting (Sillago japonica) specimens collected from different latitudinal locations along the coastal waters of China and Japan to detect possible thermal adaptations. Using population genomics, a total of 5.48 million single nucleotide polymorphisms (SNPs) from five populations revealed a complete genetic break between the Chinese and Japanese groups, which was attributed to both geographic distance and local adaptation. The shared natural selection genes between two isolated populations (i.e., Zhoushan and Ise Bay/Tokyo Bay) indicated possible parallel evolution at the genetic level induced by temperature. These genes also indicated that the process of temperature selection on isolated populations is repeatable. Moreover, we observed natural candidate genes related to membrane fluidity, possibly underlying adaptation to cold environmental stress. These findings advance our understanding of the genetic mechanisms underlying the rapid adaptations of fish species. Species distribution projection models suggested that the Chinese and Japanese groups may have different responses to future climate change, with the former expanding and the latter contracting. The findings of this study enhance our understanding of genetic differentiation and adaptation to changing environments.
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Key words:
- Sillago japonica /
- Local adaptation /
- Climate change /
- Temperature stress /
- Whole-genome resequencing
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Figure 1. Map of sampling locations and population genomic analyses of Sillago japonica
A: Map of sampling locations. Annual sea surface temperature is indicated. B: Genome-wide distribution of nucleotide diversity in 40 kb non-overlapping windows. C: Admixture analysis of five S. japonica populations. Length of each colored segment represents proportion of individual genome inferred from ancestral populations (K=2–6). D: Principal components 1 (27.80%) and 2 (16.95%) for 49 S. japonica individuals. E: Neighbor-joining tree constructed using p-distances of 49 S. japonica individuals. For abbreviations, see Table 1.
Figure 2. Isolation by distance, demographic history, and pattern of population splits
A, B: Plot of pairwise estimates of FST/(1−FST) versus two types of geographic distance (i.e., coastal and oceanic distances) between populations. C: Demographic history for each population inferred from PSMC analysis. D, E: Pattern of population splits and mixture between five S. japonica populations. Drift parameter is proportional to Ne generations, where Ne is effective population size. Scale bar shows average standard error of estimated entries in sample covariance matrix.
Figure 3. Genomic regions with strong selective signals in populations of S. japonica
A: Distribution of log2(θπ ratios) and FST values calculated in 40 kb sliding windows with 20 kb increments between RS/ZS populations (ZS as control group). Data points in red (corresponding to top 5% of empirical log2[θπ ratio] distributions with values of >0.1204 and top 5% of FST distributions with values of >0.0904) are genomic regions under selection in RS population. B: Overlapping candidate genes in RS/ZS and RS/ST pairs based on Venn diagram. C: Overlapping candidate genes in ZS/RS and Japan/RS pairs based on Venn diagram. D: Allele frequency of one SNP within cold-temperature adaptation gene Picalm across five S. japonica populations, red and blue represent two types of bases at this locus. E: Allele frequencies of one SNP within warm-temperature adaptation gene SORCS3 across five S. japonica populations, red and blue represent two types of bases at this locus.
Figure 4. PCA based on SNPs located in candidate genes and top 20 enriched KEGG pathways in candidate genes
A: PCA based on cold-temperature adaptation genes. B: PCA based on warm-temperature adaptation genes. C: KEGG enrichment for cold-temperature adaptation genes. D: KEGG enrichment for warm-temperature adaptation genes.
Figure 5. Predicted potential distribution (A, B), changes in habitat suitability (C) of Chinese group under RCP45 scenarios, and response curves of predicted occurrence probability (D) of Chinese group against temperature. Predicted potential distribution (E, F), changes in habitat suitability (G) of Japanese group under RCP45 scenarios, and response curves of predicted occurrence probability (H) of Japanese group against temperature
Table 1. Population samples of Sillago japonica used in this study
Sample location Sample ID Date of collection Sample size (n) Nucleotide diversity January
temperature (°C)Mean
temperature (°C)July
temperature (°C)Range (°C) Rushan RS August 2016 10 0.0246±0.0138 7.01 14.9 25.8 18.79 Zhoushan ZS June 2016 9 0.0212±0.0120 12.7 19.1 28.1 15.43 Santou ST July 2016 10 0.02150±0.0113 24.5 25.2 29.1 4.62 Ise Bay IB January 2009 10 0.0208±0.0108 13.5 21.3 27.3 13.75 Tokyo Bay TB October 2009 10 0.0213±0.0107 13.0 20.4 27.2 14.14 Total 49 
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