Sandrine Meylan

Stress and Body Condition as Prenatal and Postnatal Determinants of Dispersal in the Common Lizard (Lacerta vivipara)

Dispersal is a complex phenomenon affected by multiple factors. Among the factors that influence dispersal in the common lizard (Lacerta vivipara), poor maternal body condition and stress are known to decrease dispersal propensity of juveniles. But the effect of individual factors on dispersal could change when several of them act concurrently or at different developmental stages. Prenatal factors can affect clutch and/or juvenile characteristics that later affect dispersal. Postnatal influences are mainly exerted on juvenile dispersal behavior. We investigated the role of body condition and stress on dispersal at a prenatal and a postnatal stage. Stress was mimicked by experimentally increasing corticosterone levels in pregnant females and recently born juveniles. We considered (1). the influence of maternal body condition and prenatal corticosterone treatment on clutch, juvenile characteristics and on dispersal behavior and (2). the influence of juvenile body condition and postnatal corticosterone treatment on juvenile dispersal behavior. There was an interaction between maternal condition and prenatal corticosterone treatment on juvenile dispersal. Dispersal decreased with maternal corticosterone increase only in juveniles from the more corpulent females, while it increased with juvenile body condition. Good maternal body condition affected clutch and juvenile characteristics favoring dispersal, while elevation of corticosterone level (stress) exerted the opposite effect. Juvenile body condition favored dispersal, while there was no effect of postnatal corticosterone treatment on juvenile dispersal propensity.

Experimental enhancement of corticosterone levels positively affects subsequent male survival.

Corticosterone is an important hormone of the stress response that regulates physiological processes and modifies animal behavior. While it positively acts on locomotor activity, it may negatively affect reproduction and social activity. This suggests that corticosterone may promote behaviors that increase survival at the cost of reproduction. In this study, we experimentally investigate the link between corticosterone levels and survival in adult common lizards (Lacerta vivipara) by comparing corticosterone-treated with placebo-treated lizards. We experimentally show that corticosterone enhances energy expenditure, daily activity, food intake, and it modifies the behavioral time budget. Enhanced appetite of corticosterone-treated individuals compensated for increased energy expenditure and corticosterone-treated males showed increased survival. This suggests that corticosterone may promote behaviors that reduce stress and it shows that corticosterone per se does not reduce but directly or indirectly increases longer-term survival. This suggests that the production of corticosterone as a response to a stressor may be an adaptive mechanism that even controls survival.

Carotenoid-based colours reflect the stress response in the common lizard.

Under chronic stress, carotenoid-based colouration has often been shown to fade. However, the ecological and physiological mechanisms that govern colouration still remain largely unknown. Colour changes may be directly induced by the stressor (for example through reduced carotenoid intake) or due to the activation of the physiological stress response (PSR, e.g. due to increased blood corticosterone concentrations). Here, we tested whether blood corticosterone concentration affected carotenoid-based colouration, and whether a trade-off between colouration and PSR existed. Using the common lizard (Lacerta vivipara), we correlatively and experimentally showed that elevated blood corticosterone levels are associated with increased redness of the lizards belly. In this study, the effects of corticosterone did not depend on carotenoid ingestion, indicating the absence of a trade-off between colouration and PSR for carotenoids. While carotenoid ingestion increased blood carotenoid concentration, colouration was not modified. This suggests that carotenoid-based colouration of common lizards is not severely limited by dietary carotenoid intake. Together with earlier studies, these findings suggest that the common lizards carotenoid-based colouration may be a composite trait, consisting of fixed (e.g. genetic) and environmentally elements, the latter reflecting the lizards PSR.

Hormonally mediated maternal effects, individual strategy and global change

A challenge to ecologists and evolutionary biologists is predicting organismal responses to the anticipated changes to global ecosystems through climate change. Most evidence suggests that short-term global change may involve increasing occurrences of extreme events, therefore the immediate response of individuals will be determined by physiological capacities and life-history adaptations to cope with extreme environmental conditions. Here, we consider the role of hormones and maternal effects in determining the persistence of species in altered environments. Hormones, specifically steroids, are critical for patterning the behaviour and morphology of parents and their offspring. Hence, steroids have a pervasive influence on multiple aspects of the offspring phenotype over its lifespan. Stress hormones, e.g. glucocorticoids, modulate and perturb phenotypes both early in development and later into adulthood. Females exposed to abiotic stressors during reproduction may alter the phenotypes by manipulation of hormones to the embryos. Thus, hormone-mediated maternal effects, which generate phenotypic plasticity, may be one avenue for coping with global change. Variation in exposure to hormones during development influences both the propensity to disperse, which alters metapopulation dynamics, and population dynamics, by affecting either recruitment to the population or subsequent life-history characteristics of the offspring. We suggest that hormones may be an informative index to the potential for populations to adapt to changing environments.

Carotenoid-based coloration, oxidative stress and corticosterone in common lizards

SUMMARY Environmental factors including stressors, health status and social context significantly affect carotenoid-based coloration. For instance, stressors may induce the diversion of carotenoids from pigmentation pathways, potentially explaining why stressed animals often exhibit reduced coloration. However, we recently showed that high blood corticosterone concentrations, which are part of the physiological stress response, are associated with increased redness of the belly in the common lizard (Lacerta vivipara). This result clearly contrasts with the findings of many studies of carotenoid-based coloration because corticosterone is believed to increase oxidative stress. Here, we examined whether these positive effects are influenced by differences in food availability. We tested the effect of high corticosterone levels on carotenoid-based coloration, antioxidant enzyme activity and oxidative damage in common lizards subject to low and high food availability. Food restriction abolished the carotenoid-based color enhancement when corticosterone concentrations in animals were high. We discuss how carotenoid-based color can honestly signal individual quality in this species and how the increased redness induced by corticosterone could be a terminal investment in an environment where long-term survival prospects are poor but not when immediate survival is endangered.

Maternal effects on offspring locomotion: influence of density and corticosterone elevation in the lizard Lacerta vivipara.

Offspring phenotype can be affected by maternal history before and during gestation. Offspring sensitivity to maternal conditions is believed to have evolved to favor preadaptation of offspring to environmental factors they are likely to encounter. Because the locomotor capacity of an individual is likely to have important fitness consequences, we examined the role of long‐term and short‐term prenatal conditions on offspring’s locomotor performance in the lizard Lacerta vivipara. To examine long‐term prenatal effects, we manipulated the density of two populations, leaving two additional populations as unmanipulated. We then collected pregnant females within these four populations (Cévennes, Massif Central, France) and kept them in the laboratory until parturition. To examine short‐term prenatal effects, we manipulated the corticosterone level of half the females within each population. We took two different measurements of offspring locomotion: sprint speed and endurance. As already documented, sprint speed was positively correlated with offspring body size. Although population density significantly affected female fecundity, neither the density manipulation nor the population of origin influenced offspring phenotype. Corticosterone administered during gestation decreased juvenile sprint speed but did not affect juvenile endurance. Furthermore, we observed that the motivation to run was influenced by maternal hormonal treatment. Juveniles born from corticosterone‐treated mothers needed more stimuli than those born from control mothers. We conclude, therefore, that the action of corticosterone on sprint speed could be more behavioral than physiological. Offspring phenotype as measured by endurance and sprint speed appeared partly under maternal control.

Ontogenic sources of variation in sexual size dimorphism in a viviparous lizard

To elucidate the developmental aspects of the evolution of sexual size dimorphism (SSD), an understanding of the sex‐specific ontogeny of body size is critical. Here, we evaluate the relative importance of genetic and environmental determinants of SSD in juvenile common lizards (Lacerta vivipara). We examined the prenatal and post‐natal effects of population density and habitat humidity on SSD, as well as the maternal effects of food availability, corticosterone level, humidity and heat regime during gestation. Analyses indicated strong prenatal and post‐natal plasticity in body size per se and yielded three main results with respect to SSD. First, SSD in juvenile common lizards matches qualitatively the SSD observed in adults. Secondly, SSD was influenced by none of the prenatal factors investigated here, suggesting poor sex‐biased maternal effects on offspring size. Thirdly, SSD was sensitive to post‐natal habitat humidity, which positively affected growth rate more strongly in females than in males. Thus, natural variation in SSD in juvenile common lizards appears to be primarily determined by a combination of sex‐biased genetic factors and post‐natal conditions. We discuss the possibility that viviparity may constrain the evolution of sex‐biased maternal effects on offspring size.

Food deprivation modifies corticosterone-dependent behavioural shifts in the common lizard

Stressful events typically induce glucocorticoid production that suppresses unnecessary physiological and behavioural functions. The glucocorticoid production also temporally activates alternative behavioural and physiological pathways. These responses are generally adaptive changes to avoid the negative effects of stressors. However, under low food availability, these behavioural and physiological modifications might lead to energetic costs. We therefore predict that these responses should not be activated when there are energetic constraints (e.g., low food availability). We experimentally tested whether food deprivation modifies corticosterone-induced behavioural and physiological responses in captive male common lizards. We measured corticosterone-induced responses in terms of body mass, metabolic rate, activity level and basking behaviour. We found that corticosterone-induced various behavioural and physiological responses which were dependent on food availability. Well-fed lizards treated with corticosterone were active earlier, and increased their basking behaviour. These behavioural modifications did not occur in food-deprived lizards. This inactivation of stress-related behavioural changes probably allows the lizard to save energy.

Physiological actions of corticosterone and its modulation by an immune challenge in reptiles

Hormones are an important interface between genome and environment, because of their ability to modulate the animals phenotype. In particular, corticosterone, the stress hormone in lizards, is known to reallocate energy from non-essential functions to affect morphological, physiological and behavioral traits that help the organism to deal with acute or chronic stressors. However, the effects of corticosterone on life history stages are still unclear primarily because of the dependence of life history stages on both internal and external factors. Using a cross-design, we tested the effect of elevated levels of exogenous corticosterone on the physiology of pregnant females in different immune contexts in a wild population of common lizards (Lacerta vivipara). Immune challenge was induced by the injection of sheep red blood cells (SRBC) and corticosterone levels were increased using a transdermal administration of corticosterone. Thereafter, reproductive traits, metabolism and cellular immune responses were measured. The elevation of corticosterone in pregnant females significantly altered reproductive and physiological performance. The corticosterone treatment decreased clutch success, juvenile size and body condition, but enhanced measures of physiological performance, such as metabolism and catalase activity. These first results reinforce the understanding of the physiological actions of corticosterone in reptiles. The data also demonstrated different direct impacts of immune challenge by SRBC on inflammatory response and antioxidant activity. The injection of SRBC stimulated the SOD activity in larger females. Finally, we demonstrated experimentally the modulation of the corticosterone action by the immune challenge on stamina and hatching date.

Experimental litter size reduction reveals costs of gestation and delayed effects on offspring in a viviparous lizard.

Experimental studies have often been employed to study costs of reproduction, but rarely to study costs of gestation. Disentangling the relative importance of each stage of the reproductive cycle should help to assess the costs and benefits of different reproductive strategies. To that end, we experimentally reduced litter size during gestation in a viviparous lizard. We measured physiological and behavioural parameters during gestation and shortly after parturition, as well as survival and growth of females and their offspring. This study showed four major results. First, the experimental litter size reduction did not significantly affect the cellular immune response, the metabolism and the survival of adult females. Second, females with reduced litter size decreased their basking time. Third, these females also had an increased postpartum body condition. As postpartum body condition is positively related to future reproduction, this result indicates a gestation cost. Fourth, even though offspring from experimentally reduced litters had similar weight and size at birth as other offspring, their growth rate after birth was significantly increased. This shows the existence of a maternal effect during gestation with delayed consequences. This experimental study demonstrates that there are some costs to gestation, but it also suggests that some classical trade-offs associated with reproduction may not be explained by gestation costs.