Thermal conditions predict intraspecific variation in senescence rate in frogs and toads.

Variation in temperature is known to influence mortality patterns in ectotherms. Even though a few experimental studies on model organisms have reported a positive relationship between temperature and actuarial senescence (i.e., the increase in mortality risk with age), how variation in climate influences the senescence rate across the range of a species is still poorly understood in free-ranging animals. We filled this knowledge gap by investigating the relationships linking senescence rate, adult lifespan, and climatic conditions using long-term capture-recapture data from multiple amphibian populations. We considered two pairs of related anuran species from the Ranidae (Rana luteiventris and Rana temporaria) and Bufonidae (Anaxyrus boreas and Bufo bufo) families, which diverged more than 100 Mya and are broadly distributed in North America and Europe. Senescence rates were positively associated with mean annual temperature in all species. In addition, lifespan was negatively correlated with mean annual temperature in all species except A. boreas In both R. luteiventris and A. boreas, mean annual precipitation and human environmental footprint both had negligible effects on senescence rates or lifespans. Overall, our findings demonstrate the critical influence of thermal conditions on mortality patterns across anuran species from temperate regions. In the current context of further global temperature increases predicted by Intergovernmental Panel on Climate Change scenarios, a widespread acceleration of aging in amphibians is expected to occur in the decades to come, which might threaten even more seriously the viability of populations and exacerbate global decline.

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

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.

Decreased winter severity increases viability of a montane frog population.

Many proximate causes of global amphibian declines have been well documented, but the role that climate change has played and will play in this crisis remains ambiguous for many species. Breeding phenology and disease outbreaks have been associated with warming temperatures, but, to date, few studies have evaluated effects of climate change on individual vital rates and subsequent population dynamics of amphibians. We evaluated relationships among local climate variables, annual survival and fecundity, and population growth rates from a 9-year demographic study of Columbia spotted frogs (Rana luteiventris) in the Bitterroot Mountains of Montana. We documented an increase in survival and breeding probability as severity of winter decreased. Therefore, a warming climate with less severe winters is likely to promote population viability in this montane frog population. More generally, amphibians and other ectotherms inhabiting alpine or boreal habitats at or near their thermal ecological limits may benefit from the milder winters provided by a warming climate as long as suitable habitats remain intact. A more thorough understanding of how climate change is expected to benefit or harm amphibian populations at different latitudes and elevations is essential for determining the best strategies to conserve viable populations and allow for gene flow and shifts in geographic range.