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 underlie 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. life span, senescence rate and recruitment) in the Columbia spotted frog Rana luteiventris along a broad temperature gradient in the western United States. 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, life span, 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 the genomic signatures of thermal adaptation. Our results showed that temperature was negatively associated with annual adult survival and reproductive life span 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.
| Original language | English |
|---|---|
| Pages (from-to) | 1222-1238 |
| Number of pages | 17 |
| Journal | Journal of Animal Ecology |
| Volume | 91 |
| Issue number | 6 |
| DOIs | |
| State | Published - Jun 2022 |
Funding
The authors thank all the fieldworkers and students who helped to collect the capture–recapture data and DNA samples. Besides authors D.S.P. and R.M.M., lead personnel in these multi‐decade efforts include Jacqueline Cupples, Janice Engle, Hallie Lingo, Kristin Lohr, Megan McGuire, Bryce Maxell, Chad Mellison, Marisa Meyer, James Munger, Teri Slatauski and Rachel Van Horne. They also thank Jeffrey Petersen and Chad Mellison for coordinating tissue sample collection for genomic analyses. Justin Welty provided climate data. Stephen Spear provided helpful comments on an earlier version of this manuscript. Hugo Cayuela was supported as a postdoctoral researcher by the Swiss National Science Foundation (SNF grant number 31003A_182265). Funding for field work was supported by Boise State University, Bureau of Land Management, Idaho Department of Fish and Game, Nevada Department of Wildlife, University of Montana, University of Nevada Reno, US Fish and Wildlife Service, US Forest Service and US Geological Survey. Funding for genomic data collection and analysis was provided by the US Fish and Wildlife Service and the Nevada Department of Wildlife. Any use of trade, firm or product names is for descriptive purposes only and does not imply endorsement by the US Government. The authors thank all the fieldworkers and students who helped to collect the capture–recapture data and DNA samples. Besides authors D.S.P. and R.M.M., lead personnel in these multi-decade efforts include Jacqueline Cupples, Janice Engle, Hallie Lingo, Kristin Lohr, Megan McGuire, Bryce Maxell, Chad Mellison, Marisa Meyer, James Munger, Teri Slatauski and Rachel Van Horne. They also thank Jeffrey Petersen and Chad Mellison for coordinating tissue sample collection for genomic analyses. Justin Welty provided climate data. Stephen Spear provided helpful comments on an earlier version of this manuscript. Hugo Cayuela was supported as a postdoctoral researcher by the Swiss National Science Foundation (SNF grant number 31003A_182265). Funding for field work was supported by Boise State University, Bureau of Land Management, Idaho Department of Fish and Game, Nevada Department of Wildlife, University of Montana, University of Nevada Reno, US Fish and Wildlife Service, US Forest Service and US Geological Survey. Funding for genomic data collection and analysis was provided by the US Fish and Wildlife Service and the Nevada Department of Wildlife. Any use of trade, firm or product names is for descriptive purposes only and does not imply endorsement by the US Government. Open Access Funding provided by Universite de Lausanne.
| Funders | Funder number |
|---|---|
| U.S. Forest Service-Retired | |
| Bureau of Land Management | |
| Idaho Department of Fish and Game | |
| Nevada Department of Wildlife | |
| University of Nevada, Reno | |
| 31003A_182265 | |
Keywords
- adaptation
- amphibian
- copy number variants
- life history
- senescence
- single nucleotide polymorphisms
- temperature
- transposable elements