Andréaz Dupoué

Influence of temperature on the corticosterone stress-response: An experiment in the Children's python (Antaresia childreni)

To cope with environmental challenges, organisms have to adjust their behaviours and their physiology to the environmental conditions they face (i.e. allostasis). In vertebrates, such adjustments are often mediated through the secretion of glucocorticoids (GCs) that are well-known to activate and/or inhibit specific physiological and behavioural traits. In ectothermic species, most processes are temperature-dependent and according to previous studies, low external temperatures should be associated with low GC concentrations (both baseline and stress-induced concentrations). In this study, we experimentally tested this hypothesis by investigating the short term influence of temperature on the GC stress response in a squamate reptile, the Childrens python (Antaresia childreni). Snakes were maintained in contrasting conditions (warm and cold groups), and their corticosterone (CORT) stress response was measured (baseline and stress-induced CORT concentrations), within 48h of treatment. Contrary to our prediction, baseline and stress-induced CORT concentrations were higher in the cold versus the warm treatment. In addition, we found a strong negative relationship between CORT concentrations (baseline and stress-induced) and temperature within the cold treatment. Although it remains unclear how cold temperatures can mechanistically result in increased CORT concentrations, we suggest that, at suboptimal temperature, high CORT concentrations may help the organism to maintain an alert state.

Intergenerational trade‐off for water may induce a mother–offspring conflict in favour of embryos in a viviparous snake

Summary Parent–offspring conflicts are likely to occur when resources are limiting either at pre- or post-natal stages due to intergenerational trade-offs over resources. Current theory posits that such conflicts may influence the evolution of parental allocation as well as reproductive modes. While energy allocation to the offspring has received considerable attention, the distribution of water – another potentially limited vital resource to both the mother and offspring – and the resulting outcomes remain grossly understudied. Here, we explored the intergenerational trade-off related to water resources in the viviparous aspic viper (Vipera aspis) by examining the effects of water deprivation on female physiology (body mass, haematocrit and osmolality), water transfer to developing embryos and reproductive performance. As a result of water deprivation, females became dehydrated, with the effects more pronounced in pregnant compared to nonreproductive females. Among pregnant females, the impacts of water deprivation on water balance were correlated with fecundity. In contrast, water deprivation had no effect on water transfer to the offspring or on reproductive performance. Our results demonstrate that, under water-constraining conditions, female water balance is compromised in favour of the developing embryos, highlighting a significant intergenerational trade-off for water. Although ectothermic reptiles are particularly tolerant in water balance perturbations, our results suggest that, like energy, water can be a conflicting resource between mother and offspring. Parent–offspring conflict over water should therefore be further investigated to better understand reproductive modes and reproductive trade-offs in terrestrial organisms.

Effect of water deprivation on baseline and stress-induced corticosterone levels in the Children's python (Antaresia childreni)

Corticosterone (CORT) secretion is influenced by endogenous factors (e.g., physiological status) and environmental stressors (e.g., ambient temperature). Heretofore, the impact of water deprivation on CORT plasma levels has not been thoroughly investigated. However, both baseline CORT and stress-induced CORT are expected to respond to water deprivation not only because of hydric stress per se, but also because CORT is an important mineralocorticoid in vertebrates. We assessed the effects of water deprivation on baseline CORT and stress-induced CORT, in Childrens pythons (Antaresia childreni), a species that experiences seasonal droughts in natural conditions. We imposed a 52-day water deprivation on a group of unfed Childrens pythons (i.e., water-deprived treatment) and provided water ad libitum to another group (i.e., control treatment). We examined body mass variations throughout the experiment, and baseline CORT and stress-induced CORT at the end of the treatments. Relative body mass loss averaged ~10% in pythons without water, a value 2 to 4 times higher compared to control snakes. Following re-exposition to water, pythons from the water-deprived treatment drank readily and abundantly and attained a body mass similar to pythons from the control treatment. Together, these results suggest a substantial dehydration as a consequence of water deprivation. Interestingly, stress-induced but not baseline CORT level was significantly higher in water-deprived snakes, suggesting that baseline CORT might not respond to this degree of dehydration. Therefore, possible mineralocorticoid role of CORT needs to be clarified in snakes. Because dehydration usually induces adjustments (reduced movements, lowered body temperature) to limit water loss, and decreases locomotor performances, elevated stress-induced CORT in water-deprived snakes might therefore compensate for altered locomotor performances. Future studies should test this hypothesis.

Postglacial recolonization in a cold climate specialist in western Europe: patterns of genetic diversity in the adder (Vipera berus) support the central-marginal hypothesis

Understanding the impact of postglacial recolonization on genetic diversity is essential in explaining current patterns of genetic variation. The central–marginal hypothesis (CMH) predicts a reduction in genetic diversity from the core of the distribution to peripheral populations, as well as reduced connectivity between peripheral populations. While the CMH has received considerable empirical support, its broad applicability is still debated and alternative hypotheses predict different spatial patterns of genetic diversity. Using microsatellite markers, we analysed the genetic diversity of the adder (Vipera berus) in western Europe to reconstruct postglacial recolonization. Approximate Bayesian Computation (ABC) analyses suggested a postglacial recolonization from two routes: a western route from the Atlantic Coast up to Belgium and a central route from the Massif Central to the Alps. This cold‐adapted species likely used two isolated glacial refugia in southern France, in permafrost‐free areas during the last glacial maximum. Adder populations further from putative glacial refugia had lower genetic diversity and reduced connectivity; therefore, our results support the predictions of the CMH. Our study also illustrates the utility of highly variable nuclear markers, such as microsatellites, and ABC to test competing recolonization hypotheses.

Physiological state influences evaporative water loss and microclimate preference in the snake Vipera aspis.

Animals typically respond to environmental variation by adjusting their physiology, behavior, or both. Ectothermic animals are particularly sensitive to microclimatic conditions and behaviorally thermoregulate to optimize physiological performance. Yet, thermoregulation can be costly and may obligate a physiological tradeoff with water loss. Presumably, this tradeoff intensifies when animals undergo necessary life-history events (e.g., pregnancy or digestion) that impose significant behavioral and physiological changes, including shifts in behavioral thermoregulation and increased metabolic rate. Thus, behavioral responses, such as modified microclimatic preferences, may help mitigate the physiological tradeoff between thermoregulation and water loss. Herein, we examined the influence of major physiological states (specifically, pregnancy, ecdysis, and digestion) on evaporative water loss and on behavioral adjustments in a viviparous snake, Vipera aspis. First, we used open-flow respirometry to measure the effects of physiological states and microclimatic conditions (temperature and humidity) on the rate of total evaporative water loss (TEWL) and metabolic rate (rate of O2 consumption, V˙O2). Then, we experimentally tested the influence of physiological state on microclimate selection. We found that energy-demanding physiological states were associated with i) an increased rate of TEWL and V˙O2 compared to control states and ii) a slight preference (statistically marginal) for both warm and humid conditions compared to controls, suggesting a state-specificity in behavioral response. Overall our results underline the impact of physiological state on water loss and demonstrate the potential for behavior to mitigate the physiological tradeoff between thermoregulation and water balance.

Water deprivation increases maternal corticosterone levels and enhances offspring growth in the snake Vipera aspis.

ABSTRACT Circulating glucocorticoid (GC) levels may increase as a result of reproductive effort or in response to unpredictable events. However, GC secretion can vary with the availability of vital trophic resources such as energy. While water represents another critical resource, the impact of water deprivation on GC secretion during reproduction has not yet been thoroughly investigated. Here, we examined the effects of water deprivation on plasma corticosterone (CORT) concentrations of female aspic vipers (Vipera aspis), and determined the impacts of water deprivation on offspring traits. We exposed both pregnant and non-reproductive females to a 20-day water deprivation and compared their pre- and post-deprivation CORT levels with those of control females. At the end of the treatment, only water-deprived pregnant females showed a significant increase in CORT levels. In pregnant females, changes in baseline CORT level were correlated with changes in female hydration state. Changes in baseline CORT levels were also negatively influenced by maternal reproductive effort in pregnant control females, while such a relationship was not apparent in pregnant water-deprived females. Finally, we found that offspring from water-deprived females had higher growth rates than offspring from control females. Offspring growth was also positively correlated with changes in both maternal osmolality and baseline CORT levels. Together, our results suggest that dehydration increases maternal CORT levels, which may subsequently influence offspring development. Further long-term field studies are therefore required to assess whether there is an adaptive significance of this response. Summary: Water deprivation induces an increase in baseline corticosterone level in pregnant aspic vipers, which may subsequently influence offspring growth.

Shorter telomeres precede population extinction in wild lizards

Identifying the early warning signals of catastrophic extinctions has recently become a central focus for ecologists, but species’ functional responses to environmental changes remain an untapped source for the sharpening of such warning signals. Telomere length (TL) analysis represents a promising molecular tool with which to raise the alarm regarding early population decline, since telomere attrition is associated with aging processes and accelerates after a recurrent exposure to environmental stressors. In the southern margin of their range, populations of the common lizard (Zootoca vivipara) recently became extinct at lowest elevations due to changes in climate conditions. However, the proximal signals involved in these demographic declines are still unknown. Here, we sampled 100 yearling lizards from 10 natural populations (n = 10 per population) along an extinction risk gradient. Relative lizard abundance dramatically dropped over 12 years in low-altitude populations characterized by warmer ambient temperatures and higher body growth of lizards early in life. A non-linear relationship was found between TL and population extinction risk, with shorter telomeres in populations facing high risk of extinction when compared to non-threatened ones. Our results identify TL as a promising biomarker and imply that population extinctions might be preceded by a loop of physiological aging.

Effects of mild wintering conditions on body mass and corticosterone levels in a temperate reptile, the aspic viper (Vipera aspis)

Temperate ectotherms are expected to benefit from climate change (e.g., increased activity time), but the impacts of climate warming during the winter have mostly been overlooked. Milder winters are expected to decrease body condition upon emergence, and thus to affect crucial life-history traits, such as survival and reproduction. Mild winter temperature could also trigger a state of chronic physiological stress due to inadequate thermal conditions that preclude both dormancy and activity. We tested these hypotheses on a typical temperate ectothermic vertebrate, the aspic viper (Vipera aspis). We simulated different wintering conditions for three groups of aspic vipers (cold: ~6 °C, mild: ~14 °C and no wintering: ~24 °C) during a one month long period. We found that mild wintering conditions induced a marked decrease in body condition, and provoked an alteration of some hormonal mechanisms involved in emergence. Such effects are likely to bear ultimate consequences on reproduction, and thus population persistence. We emphasize that future studies should incorporate the critical, albeit neglected, winter season when assessing the potential impacts of global changes on ectotherms.

Water restriction causes an intergenerational trade‐off and delayed mother–offspring conflict in a viviparous lizard

Summary 1.Parenting is costly and because the relationship between the mother and embryos is not mutualistic, mother-offspring conflicts may exist whenever resource are scarce. However, intergenerational trade-offs and conflicts resulting from limited access to water, a vital and depreciable resource, remain largely overlooked. 2.In this study, we examined the physiological, reproductive and life history responses to water restriction in the European Common Lizard (Zootoca vivipara). We hypothesised that, under water-limited conditions, pregnant females experience both short-term and long-term physiological impacts (dehydration and stress) underlying an allocation trade-off for water between mothers and offspring. 3.Water restriction led to a decrease in body mass, and an increase in plasma osmolality (dehydration) and corticosterone concentration in both males and females. The extent of the dehydration was positively correlated with fecundity in females. This suggests a trade-off between maternal water balance and allocation of water to developing embryos during reproduction. 4.Water restriction had no immediate effect on reproductive output or offspring morphology at birth. Yet, water restriction in pregnant females enhanced their reproductive effort the following year but reduced the early life growth and annual survival of their second-year offspring. 5.These delayed fitness responses to water restriction in offspring and mothers suggest that water can trigger intergenerational conflicts as demonstrated for energy. Although the mediation of this conflict remains to be clarified, we hypothesized that it represents a selective force that influences reproductive strategies. This article is protected by copyright. All rights reserved.

Oxidative stress in a capital breeder (Vipera aspis) facing pregnancy and water constraints

ABSTRACT The physiological mechanisms underlying the ‘cost of reproduction’ remain under debate, though oxidative stress has emerged as a potential candidate. The ‘oxidative cost of reproduction’ has received considerable attention with regards to food and antioxidant availability; however, the limitation of water availability has thus far been neglected. In this study, we experimentally examined the combined effect of pregnancy and water deprivation on oxidative status in a viviparous snake (Vipera aspis), a species naturally exposed to periods of water and food deprivation. We predicted a cumulative effect of pregnancy and dehydration on oxidative stress levels. Our results support the occurrence of an oxidative cost of reproduction as we found higher oxidative damage levels in pregnant females than in non-reproductive individuals, despite an up-regulation of antioxidant defences. Surprisingly, water deprivation was associated with an up-regulation of antioxidant defences, and did not increase oxidative damage, either alone or in combination with reproduction. Summary: Pregnancy in aspic vipers is associated with increased oxidative damage levels despite an up-regulation of antioxidant defences; dehydration triggers an up-regulation of antioxidant defences, so preventing a cumulative effect of reproduction and dehydration.