Genomic signatures of thermal adaptation are associated with clinal shifts of life history in a broadly distributed frog.

Abstract

Temperature is a critical driver of ectotherm life history strategies, whereby a warmer environment is associated with increased growth, reduced longevity, and accelerated senescence. Increasing evidence indicates that thermal adaptation may underly such life history shifts in wild populations. Single Nucleotide Polymorphisms (SNPs) and Copy Number Variants (CNVs) can help uncover the molecular mechanisms of temperature-driven variation in growth, longevity, and senescence. However, our understanding of these mechanisms is still limited, which reduces our ability to predict the response of non-model ectotherms to global temperature change. 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.