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.

Studies of age-specific changes in mortality have emphasized that actuarial senescence (i.e., the increase in mortality with age; called “senescence” hereafter) patterns are extremely diverse in the wild (1–3). To date, most studies have been conducted in birds and mammals and have demonstrated that the age at the onset of senescence (4, 5), the rate of senescence (1, 6), and the overall shape of mortality patterns (7, 8) all vary across species. Variation in senescence patterns across species is broadly explained by phylogeny (6), body size (1), and the pace of life (4). Although the genetic and physiological mechanisms modulating among-species variation in senescence are still poorly understood (9), empirical evidence accumulated so far shows that senescence is a ubiquitous phenomenon whose form and intensity vary considerably across the tree of life.In contrast, much less research has focused on variation in senescence patterns across populations within a given species (3). This requires intensive long-term monitoring of multiple populations across a species’ range, which is uncommon. Studies comparing captive and wild populations have shown that controlled environments in zoos slow down the senescence process in mammals (10), with deceleration more pronounced in short-lived than in long-lived species (11). Variation in age-dependent mortality patterns between populations of a given species has also been reported in the wild, suggesting that local environmental conditions (e.g., anthropogenic disturbance, habitat quality) may affect senescence patterns (12–14). However, the influence of environmental variation on the intensity of senescence is still poorly understood in most animal clades (3).Climatic conditions might be a key factor driving intraspecific variation in senescence (15, 16), especially in ectotherms, because their metabolism, activity patterns, and lifespan all strongly depend on temperature (17, 18). Studies of both natural and experimental populations of invertebrates and ectothermic vertebrates have so far revealed that lifespan decreases with increasing ambient temperature (15, 16). In short-lived model organisms, the decrease in lifespan at high temperature is associated with accelerated senescence under laboratory conditions [Caenorhabditis elegans (19), Drosophila melanogaster (20), and Nothobranchius furzeri (21)]. However, lifespan is a trait only partially correlated to senescence rate [e.g., R² < 0.50 in mammals (22)], which does not reliably reflect age-specific mortality patterns (9). To date, a link between senescence and climate has not been demonstrated in the wild, which limits our ability to assess the universality of this relationship and prevents reliable predictions about the influence of climate change on senescence.Amphibians are excellent biological models to investigate the influence of climatic conditions on senescence patterns in nature. Previous studies have shown that as temperatures decrease along altitudinal and latitudinal gradients, the pace of life of amphibians slows down, involving delayed sexual maturity, less frequent egg deposition by females, and increased lifespan (23, 24); this slow pace of life is expected given the ecological effects of altitude in most taxa (25). At higher altitudes and latitudes, individuals maximize survival in cold conditions by reducing their activity period and placing themselves into an hypometabolic state that minimizes their energy expenditure (26, 27). At lower altitudes and latitudes, the activity period is longer (23); overall, metabolic activity increases, and warm conditions both diminish mitochondrial efficiency and accelerate the accumulation of oxidative damages (28), possibly leading to an earlier or faster senescence. This effect may be amplified by evaporative water loss that reduces the capacity of cutaneous respiration (29) and body temperature regulation (30) when individuals experience hot temperatures and low precipitation. These phenomena could have synergistic effects on age-dependent mortality, resulting in an acceleration of senescence with increasing temperature and decreasing precipitation.To assess the relationship between age-specific mortality patterns and climatic conditions, we measured the influence of temperature and precipitation on among-population variation in senescence rate and adult lifespan in two pairs of frog and toad species from the Ranidae and Bufonidae families, which diverged more than 100 Mya (31). We focused on four species widely distributed in North America (Columbia spotted frog, Rana luteiventris, and Boreal toad, Anaxyrus boreas; Fig. 1) and Europe (common frog, Rana temporaria, and common toad, Bufo; Fig. 1). To perform these analyses, we took advantage of long-term capture–recapture (CR) data collected in 16 populations of R. luteiventris and A. boreas (eight per species) distributed along a broad climatic gradient in the western United States (Fig. 1 and SI Appendix, Table S1) and in four populations of R. temporaria and B. bufo (two per species) experiencing contrasted temperature conditions in Europe (Fig. 1 and SI Appendix, Table S1). More specifically, we tested whether warmer mean annual temperature was associated with higher senescence rate and shorter adult lifespan and, similarly, if higher mean annual precipitation was correlated with lower senescence rate and longer adult lifespan. As human activities may also influence local mortality patterns in amphibians (13, 32), we took into account the intensity of human footprint by including a quantitative, empirically based measure of ecological integrity in our models (33) (more details about this metric are given in SI Appendix, Supplementary analysis 1). Furthermore, as sexes may differ in terms of mortality patterns (6, 34) and physiological response to thermal stress, we tested whether the association among senescence, lifespan, and climatic conditions differed between males and females.Open in a separate windowFig. 1.Study system used to test the links among actuarial senescence rate, lifespan, and climatic conditions in four amphibian species from North America (Columbia spotted frog, R. luteiventris, and Boreal toad, A. boreas) and Europe (common frog, R. temporaria, and common toad, B. bufo). (A) Calibrated phylogenetic tree (retrieved from ref. 63, http://www.timetree.org/) presenting the phylogenetic relationships and divergence time among the four species; the African clawed frog (Xenopus laevis) was used as an outgroup. (B and C) Maps with background showing mean annual temperature (A) and mean annual precipitation (B) in the western United States (extracted from https://adaptwest.databasin.org). (D and E) Maps with background showing mean annual temperature (D) and mean annual precipitation (E) in Europe (extracted from https://www.worldclim.org/).