Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.
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.
Sex‐related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture–recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex‐specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the “unguarded X/Z effect”) or repeat‐rich Y/W chromosome (the “toxic Y/W effect”) could accelerate aging in the heterogametic sex in some vertebrate clades.
Strong phenological shifts in response to changes in climatic conditions have been reported for many species, including amphibians, which are expected to breed earlier. Phenological shifts in breeding are observed in a wide number of amphibian populations, but less is known about populations living at high elevations, which are predicted to be more sensitive to climate change than lowland populations. The goal of this study is to assess the main factors determining the timing of breeding in an alpine population of the common toad (Bufo bufo) and to describe the observed shifts in its breeding phenology. We modelled the effect of environmental variables on the start and peak dates of the breeding season using 39 years of individual-based data. In addition, we investigated the effect of the lunar cycle, as well as the individual variation in breeding phenology. Finally, to assess the individual heterogeneity in the timing of breeding, we calculated the repeatability of the timing of arrival at the breeding site. Breeding advanced to earlier dates in the first years of the study but the trend continued only until the mid 1990s, and stabilised afterwards. Overall, toads are now breeding on average around 30 days earlier than at the start of the study period. High temperatures and low snow cover in winter and spring, as well as reduced spring precipitation were all associated with earlier breeding. Additionally, we found evidence of males arriving on average before females at the breeding site but no clear and strong effect of the lunar cycle. We only found weak evidence of among-individual variation in shifts in the breeding phenology, as well as a low repeatability of arrival timing. Our findings show that the observed changes in breeding phenology are strongly associated with the environmental conditions. These results contribute to filling a knowledge gap on the effects of climate change on alpine amphibian populations. Moreover, we show that changes in phenology, especially in the mountains, can be hard to predict as local microclimatic conditions do not necessarily reflect the observed global climatic trends.
Temporal variation in vital rates (e.g., survival, reproduction) can decrease the long-term mean performance of a population. Species are therefore expected to evolve demographic strategies that counteract the negative effects of vital rate variation on the population growth rate. One key strategy, demographic buffering, is reflected in a low temporal variation in vital rates critical to population dynamics. However, comparative studies in plants have found little evidence for demographic buffering, and little is known about the prevalence of buffering in animal populations. Here, we used vital rate estimates from 31 natural populations of 29 animal species to assess the prevalence of demographic buffering. We modeled the degree of demographic buffering using a standard measure of correlation between the standard deviation of vital rates and the sensitivity of the population growth rate to changes in such vital rates across populations. We also accounted for the effects of life-history traits, i.e., age at first reproduction and spread of reproduction across the life cycle, on these correlation measures. We found no strong or consistent evidence of demographic buffering across the study populations. Instead, key vital rates could vary substantially depending on the specific environmental context populations experience. We suggest that it is time to look beyond concepts of demographic buffering when studying natural populations towards a stronger focus on the environmental context-dependence of vital-rate variation.
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