When carapace governs size: variation among age classes and individuals in a free-ranging ectotherm with delayed maturity.

Juvenile growth strongly impacts life-history traits during adulthood. Yet, in juveniles with delayed maturity, elusiveness has hindered age-specific studies of growth, precluding any detailed research on its consequences later in life. Different complex growth patterns have been extracted from captive animals, suggesting species-specific trajectories occur in free-ranging animals. How pronounced are growth and body size variation (VBS) throughout a long-lived ectotherm's life? Is VBS constant among age classes prior to maturity, or do compensatory and/or cumulative effects driven by long-lived-animal-specific strategies create distinct VBS cohorts, to ensure survival? To tackle the issue, we modelled growth data from continuous and dense annual capture-mark-recapture sampling (5096 body measurements of 1134 free-ranging individuals) of both immature and mature, long-lived Hermann's tortoises. We analysed population, cohort, and individual-based growth and VBS. Growth ring inferred ages were cross validated with annual recaptures in 289 juveniles. Analyses unravelled an S-shaped growth curve and identified three age cohorts across which VBS increases in a step-wise manner. Neonate-specific constraints and compensatory effects seem to control VBS until 4 years of age, possibly promoting survival with size. Subsequently, a hardened carapace takes over and cumulative effects fuelled by faster growth progressively increase VBS. Whereas ungulates are in a hurry to attain adult size before growth ceases (minimizing VBS), indeterminately growing tortoises can shape individual asymptotic sizes even after growth decelerates. Tortoise size is clearly shaped by age-specific ecological constraints; interestingly, it is likely the carapace that conducts the strategy, rather than maturity per se.

Contrasting patterns of environmental fluctuation contribute to divergent life histories among amphibian populations.

Because it modulates the fitness returns of possible options of energy expenditure at each ontogenetic stage, environmental stochasticity is usually considered a selective force in driving or constraining possible life histories. Divergent regimes of environmental fluctuation experienced by populations are expected to generate differences in the resource allocation schedule between survival and reproductive effort and outputs. To our knowledge, no study has previously examined how different regimes of stochastic variation in environmental conditions could result in changes in both the temporal variation and mean of demographic parameters, which could then lead to intraspecific variation along the slow-fast continuum of life history tactics. To investigate these issues, we used capture-recapture data collected on five populations of a long-lived amphibian (Bombina variegata) experiencing two distinct levels of stochastic environmental variation: (1) constant availability of breeding sites in space and time (predictable environment), and (2) variable spatio-temporal availability of breeding sites (unpredictable environment). We found that female breeding propensity varied more from year to year in unpredictable than in predictable environments. Although females in unpredictable environments produced on average more viable offspring per year, offspring production was more variable between years. Survival at each ontogenetic stage was slightly lower and varied significantly more from year to year in unpredictable environments. Taken together, these results confirm that increased environmental stochasticity can modify the resource allocation schedule between survival and reproductive effort and outputs and may lead to intraspecific variation along the slow-fast continuum of life history tactics.

Does habitat unpredictability promote the evolution of a colonizer syndrome in amphibian metapopulations?

Dispersal is a central component of life history evolution. An increasing number of studies suggest that spatiotemporally variable environments may promote the evolution of "dispersal syndromes," consisting of covariation patterns between dispersal and morphological, physiological, behavioral, and life history traits. At the interspecific scale, the "colonizer syndrome" appears to be one of the most frequently recorded associations between dispersal and life history traits, linking a high dispersal rate, high fecundity, and a short lifespan as systematically combined adaptations in spatiotemporally varying environments. However, few studies have highlighted the existence of a "colonizer syndrome" at the intraspecific scale, and none have investigated how different degrees of habitat stochasticity might shape covariation patterns between dispersal and life history traits. In this study, we examined this issue in free-ranging metapopulations of the yellow-bellied toad (Bombina variegata) using capture-recapture data. Combining the results of this study with another recent study, we found that a high dispersal rate, high fecundity, and a short lifespan are associated in metapopulations experiencing unpredictable environments. In contrast, a very low dispersal rate (close to zero), low fecundity and a long lifespan are associated in metapopulations occupying predictable environments. We discuss these results as well as their demographic and evolutionary consequences.

Demographic responses to weather fluctuations are context dependent in a long-lived amphibian.

Weather fluctuations have been demonstrated to affect demographic traits in many species. In long-lived organisms, their impact on adult survival might be buffered by the evolution of traits that reduce variation in interannual adult survival. For example, skipping breeding is an effective behavioral mechanism that may limit yearly variation in adult survival when harsh weather conditions occur; however, this in turn would likely lead to strong variation in recruitment. Yet, only a few studies to date have examined the impact of weather variation on survival, recruitment and breeding probability simultaneously in different populations of the same species. To fill this gap, we studied the impact of spring temperatures and spring rainfall on survival, on reproductive skipping behavior and on recruitment in five populations of a long-lived amphibian, the yellow-bellied toad (Bombina variegata). Based on capture-recapture data, our findings demonstrate that survival depends on interactions between age, population and weather variation. Varying weather conditions in the spring result in strong variation in the survival of immature toads, whereas they have little effect on adult toads. Breeding probability depends on both the individual's previous reproductive status and on the weather conditions during the current breeding season, leading to high interannual variation in recruitment. Crucially, we found that the impact of weather variation on demographic traits is largely context dependent and may thus differ sharply between populations. Our results suggest that studies predicting the impact of climate change on population dynamics should be taken with caution when the relationship between climate and demographic traits is established using only one population or few populations. We therefore highly recommend further research that includes surveys replicated in a substantial number of populations to account for context-dependent variation in demographic processes.

Ontogeny, not prey availability, underlies allopatric venom variability in insular and mainland populations of Vipera ammodytes.

Allopatric populations living under distinct ecological conditions are excellent systems to infer factors underlying intraspecific venom variation. The venom composition of two populations of Vipera ammodytes, insular with a diet based on ectotherms and mainland with a diet based on ectotherms and endotherms, was compared considering the sex and age of individuals. Ten toxin families, dominated by PLA2, svMP, svSP, and DI, were identified through a bottom-up approach. The venom profiles of adult females and males were similar. Results from 58 individual SDS-PAGE profiles and venom pool analysis revealed significant differences between juveniles compared to subadults and adults. Two venom phenotypes were identified: a juvenile svMP-dominated and KUN-lacking phenotype and an adult PLA2/svMP-balanced and KUN-containing phenotype. Despite differences in prey availability (and, therefore, diet) between populations, no significant differences in venom composition were found. As the populations are geographically isolated, the lack of venom diversification could be explained by insufficient time for natural selection and/or genetic drift to act on the venom composition of island vipers. However, substantial differences in proteomes were observed when compared to venoms from geographically distant populations inhabiting different conditions. These findings highlight the need to consider ecological and evolutionary processes when studying venom variability. SIGNIFICANCE: This study provides the first comprehensive analysis of the venom composition of two allopatric populations of Vipera ammodytes, living under similar abiotic (climate) but distinct biotic (prey availability) conditions. The ontogenetic changes in venom composition, coupled with the lack of differences between sex and between populations, shed light on the main determinants of venom evolution in this medically important snake. Seven new proteomes may facilitate future comparative studies of snake venom evolution. This study highlights the importance of considering ecological and evolutionary factors to understand snake venom variation.

Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity.

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.

Inside the shell: body composition of free-ranging tortoises (Testudo hermanni).

Body condition indices (BCI - mass scaled by size) are widely used in ecological studies. They presumably reflect variations of endogenous fat reserves in free-ranging animals. In the field, however, accurately quantifying internal body reserves is a difficult task. This is especially true in armoured animals where convenient clues that may guide BCI assessment (e.g. visible subcutaneous fat deposits) remain inaccessible. Alternatively, inclusive dissections may provide anatomical abacuses to estimate body reserves in living individuals. Sacrificing animals for this purpose is not acceptable. We opportunistically tested the ability of BCI to estimate body reserves in 13 free-ranging Hermann's tortoises (Gmelin, 1789) dissected soon after they died from natural causes. On average, BCI values were lower in dissected tortoises relative to living individuals (N > 10,000 measurements), but they remained within the range of variation of the studied populations. Shell mass relative to body mass was high and showed considerable inter-individual variation (33.5% to 52.3%). Stomach and digestive tract content represented another important and variable part of total body mass (4.4% to 14.5%). The contribution of fat bodies was negligible (0.0% to 0.5%). Overall, in the studied tortoises, variations of body condition are weakly determined by variations of fat stores. Other endogenous (e.g. muscles, visceral tissues, liver) and "exogenous" (e.g. digestive tract content, clutch) elements should be considered to better understand age and sex specific life-history trade-offs faced by chelonians.