Genomic data of Columbia spotted frog (Rana luteiventris)

In this study, we examined the potential role of thermal adaptation in clinal shifts of life history traits (i.e., lifespan, senescence rate, and recruitment) in the Columbia spotted frog (Rana luteiventris) along a broad temperature gradient in the western USA. We took advantage of extensive capture-recapture datasets of 20,033 marked individuals from eight populations surveyed annually for 14 – 18 years to examine how mean annual temperature and precipitation influenced demographic parameters (i.e., adult survival, lifespan, senescence rate, recruitment, and population growth). After showing that temperature was the main climatic predictor influencing demography, we used RAD-seq data (50,829 SNPs and 6,599 putative CNVs) generated for 352 individuals from 31 breeding sites to identify genomic signatures of thermal adaptation. Our results showed that temperature was negatively associated with annual adult survival and reproductive lifespan and positively associated with senescence rate. By contrast, recruitment increased with temperature, promoting the long-term viability of most populations. These temperature-dependent demographic changes were associated with strong genomic signatures of thermal adaptation. We identified 148 SNP candidates associated with temperature including three SNPs located within protein-coding genes regulating resistance to cold and hypoxia, immunity, and reproduction in ranids. We also identified 39 CNV candidates (including within 38 transposable elements) for which normalized read depth was associated with temperature. Our study indicates that both SNPs and structural variants are associated with temperature and could eventually be found to play a functional role in clinal shifts in senescence rate and life history strategies in R. luteiventris. These results highlight the potential role of different sources of molecular variation in the response of ectotherms to environmental temperature variation in the context of global warming.

本研究以美国西部广泛温度梯度分布下的哥伦比亚斑点蛙（Columbia spotted frog，*Rana luteiventris*）为研究对象，探讨了热适应在其生活史性状（即寿命、衰老速率与种群补充量）渐变群变化中的潜在作用。本研究利用覆盖8个种群的大规模标记重捕数据集，该数据集包含20033只标记个体，且对这些种群开展了14至18年的年度监测，以分析年平均气温与降水量对种群统计参数（即成体存活率、寿命、衰老速率、种群补充量及种群增长）的影响。在证实气温是影响种群统计动态的主要气候预测因子后，我们使用来自31个繁殖位点的352个个体的限制性位点相关DNA测序（RAD-seq）数据（包含50829个单核苷酸多态性（Single Nucleotide Polymorphisms，SNPs）以及6599个推定拷贝数变异（Copy Number Variations，CNVs）），以识别热适应的基因组特征。研究结果显示，气温与年度成体存活率和生殖寿命呈负相关，而与衰老速率呈正相关。与之相反，种群补充量随气温升高而增加，这促进了多数种群的长期存续能力。这些依赖于气温的种群统计变化与显著的热适应基因组特征密切相关。我们共鉴定出148个与气温相关的候选SNPs，其中3个位于调控蛙科动物抗寒与抗缺氧能力、免疫及繁殖的蛋白质编码基因内。此外还鉴定出39个与气温相关的候选CNVs（其中38个位于转座因子内），其标准化读长深度与气温存在显著关联。本研究表明，SNPs与结构变异均与气温相关，且未来或可证实二者在哥伦比亚斑点蛙的衰老速率及生活史策略渐变群变化中发挥功能性作用。这些研究结果凸显了在全球变暖背景下，不同来源的分子变异在变温动物应对环境温度变化的响应中所具备的潜在重要作用。