In Memoriam : Barry Sinervo 1961-2021

Peer reviewedPublisher PD

Climate change and a little brown lizard: the impact of climate on maternal thermoregulation, offspring phenotype, and host-parasite interactions in the viviparous European common lizard (Zootoca vivipara)

Climate change is predicted to severely impact species distributions and extinction risk in the coming decades. Ectotherms, such as lizards, are of particular concern due to their dependence on environmental temperatures to survive and reproduce. The predictions of extreme weather events and increases in global mean temperatures will affect the ability of these organisms to carry out important functions such as feeding or breeding. While we predict that these organisms will face challenges from climate change, examining whether they show evidence of coping with these changes is critical for determining extinction risk and making conservation decisions. In this dissertation, I use treatments of 3-hour (short), 6-hour (mid/control), and 9-hour (long) access to basking heat to investigate how different climate extremes, predicted to increase and worsen under climate change, would impact various aspects of pregnant viviparous European common lizards (Zootoca vivipara). The 3-hour treatments reflect an unusually long series of cool days limiting thermoregulation, 6-hours reflects the “normal” period of contemporary climate and 9-hours reflects periods of long-duration heat spells. In Chapter 1, I look at the flexibility of females to modify their behavior to different basking treatments and how intraspecific variation between populations plays a role. My results demonstrate these lizards exhibit plasticity in basking behavior in response to varying thermal opportunity. However, the magnitude to which they modify their behavior is significantly tempered by environmental characteristics of their population of origin. In Chapter 2, I investigate how basking treatments influence gestation and offspring phenotype, as the offspring life history stage is one of great importance. We found that offspring phenotype was significantly affected by mother basking treatments with local population differences and sex-dependent outcomes on size and viability in juveniles. My findings indicate that cooler and warmer temperatures have different effects on progeny phenotype and may have cascading impacts under climate change in the next generation. In Chapter 3, I examine how parasite load varies between populations and whether basking treatments influence a lizard’s ability to fight infection. The basking treatments influenced changes in parasite load in three of the five populations, where we observed a relatively small increase in parasite abundance in lizards in the short and mid/control basking treatment compared to the long treatment. This difference between populations suggests a context-dependent impact of basking opportunities on the capability of lizards to clear parasite infections, under the warm environment treatment (9-h) and provides further evidence that ectothermic host-blood parasite relationships are likely to be impacted by future and contemporary climate change. The results of this dissertation ultimately highlight the complex impacts climate change can have on these organisms and will hopefully encourage further research while raising awareness of this pressing issue

The first ecological study on the oldest allochthonous population of European cave salamanders (Hydromantes sp.)

International audienceThe introduction of allochthonous species often represents a serious problem for ecosystems and native species. Usually, these cases involve common widespread species that show high adaptability and strong competitiveness against local species. Within amphibians, the introduction of allochthonous species mainly deals with anurans, while cases involving caudata are few and poorly studied. We report the first assessment of an introduced population of European plethodontid salamanders. This population is located in the French Pyrenees and represents the oldest allochthonous Hydromantes population. We reconstructed the history of its introduction and collected data on the ecology and feeding habits of this population. Our results show that this population is stable and reproductive, showing strong similarities to Italian mainland species of Hydromantes. This study provided the base for further studies focused on this allochthonous population of European cave salamanders

To cool or not to cool? Intestinal coccidians disrupt the behavioral hypothermia of lizards in response to tick infestation

It is generally accepted that parasites exert negative effects on their hosts and that natural selection favors specific host responses that mitigate this impact. It is also known that some components of the host immune system often co-evolve with parasite antigens resulting in a host-parasite arms race. In addition to immunological components of the anti-parasitic response, host behavioral responses are also important in this arms race and natural selection may favor avoidance strategies that preclude contact with parasites, or shifts in the host's thermoregulatory strategy to combat active infections (e.g., behavioral fever). Ticks are widespread parasites with direct and indirect costs on their vertebrate hosts. Their saliva provokes hemolysis in the blood of their hosts and can transmit a plethora of tick-borne pathogens. We enquired whether tick infestation by Ixodes pacificus can provoke a thermoregulatory response in Sceloporus occidentalis. For this, we compared the thermoregulatory behavior of tick-infested lizards against tick-infested lizards co-infected with two different species of coccidians (Lankesterella occidentalis and Acroeimeria sceloporis). After this, lizards were kept in individual terraria with a basking spot and fed ad libitum. We found that tick-infested lizards sought cooler temperatures in proportion to their tick load, and this response was independent of the co-infection status by L. occidentalis. This was consistent in April and June (when tick loads were significantly lower) and suggests a conservative strategy to save energy which might have been selected to overcome tick infestations during phenological peaks of this parasite. However, this behavior was not observed in lizards co-infected with A. sceloporis, suggesting that co-infection with this intestinal parasite prompt lizards to be active. Cost of tick infestation was confirmed because housed lizards lost weight at a constant ratio to initial tick load, independently of other infections. The broader implications of these findings are discussed in the context of climate change.Research at UCSC was supported by an NSF grant (EF-1241848 to BS). Spanish Ministerio de Economía y Competitividad provided support (BES-2010-038427 and EEBB-I-14-08326 to RM-P)

Climate dependent heating efficiency in the common lizard

International audienceRegulation of body temperature is crucial for optimizing physiological performance in ectotherms but imposes constraints in time and energy. Time and energy spent thermoregulating can be reduced through behavioral (e.g., basking adjustments) or biophysical (e.g., heating rate physiology) means. In a heterogeneous environment, we expect thermoregulation costs to vary according to local, climatic conditions and therefore to drive the evolution of both behavioral and biophysical thermoregulation. To date, there are limited data showing that thermal physiological adjustments have a direct relationship to climatic conditions. In this study, we explored the effect of environmental conditions on heating rates in the common lizard (Zootoca vivipara ). We sampled lizards from 10 populations in the Massif Central Mountain range of France and measured whether differences in heating rates of individuals correlated with phenotypic traits (i.e., body condition and dorsal darkness) or abiotic factors (temperature and rainfall). Our results show that heat gain is faster for lizards with a higher body condition, but also for individuals from habitats with higher amount of precipitation. Altogether, they demonstrate that environmentally induced constraints can shape biophysical aspects of thermoregulation

Multiple color patches and parasites in Sceloporus occidentalis: Differential relationships by sex and infection

Parasites generally have a negative influence on the color expression of their hosts. Sexual selection theory predicts resistant high-quality individuals should show intense coloration, whereas susceptible low-quality individuals would show poor coloration. However, intensely colored males of different species of Old and New World lizards were more often infected by hemoparasites. These results suggest that high-quality males, with intense coloration, would suffer higher susceptibility to hemoparasites. This hypothesis remains poorly understood and contradicts general theories on sexual selection. We surveyed a population of Sceloporus occidentalis for parasites and found infections by the parasite genera Lankesterella and Acroeimeria. In this population, both males and females express ventral blue and yellow color patches. Lankesterella was almost exclusively infecting males. The body size of the males significantly predicted the coloration of both blue and yellow patches. Larger males showed darker (lower lightness) blue ventral patches and more saturated yellow patches that were also orange-skewed. Moreover, these males were more often infected by Lankesterella than smaller males. The intestinal parasite Acroeimeria infected both males and females. The infection by intestinal parasites of the genus Acroeimeria was the best predictor for the chroma in the blue patch of the males and for hue in the yellow patch of the females. Those males infected by Acroeimeria expressed blue patches with significantly lower chroma than the uninfected males. However, the hue of the yellow patch was not significantly different between infected and uninfected females. These results suggest a different effect of Lankesterella and Acroeimeria on the lizards. On the one hand, the intense coloration of male lizards infected by Lankesterella suggested high-quality male lizards may tolerate it. On the other hand, the low chroma of the blue coloration of the infected males suggested that this coloration could honestly express the infection by Acroeimeria.Financial support was provided by Spanish Ministerio de Economía y Competitividad (projects CGL2012-40026-C02-01 and CGL2015-67789-C2-1-P (MINECO/FEDER) to SM, and CGL2012-40026-C02-02 to JM, and grant numbers BES-2010-038427 and EEBB-I-14-08326 to RM-P). Ministerio de Educación funded SR with FPU grant number AP-2009-1325 and EST13/00196. Permits for carrying out this investigation and collecting lizards were provided by the UCSC ethics committee (IACUC) and CDFG to RDC. Research at the UCSC was supported by an NSF grant to BS (EF-1241848).Peer Reviewe

Reduction in baseline corticosterone secretion correlates with climate warming and drying across wild lizard populations

International audienceClimate change should lead to massive loss of biodiversity in most taxa, but the detailed physiological mechanisms underlying population extinction remain largely elusive so far. In vertebrates, baseline levels of hormones such as glucocorticoids (GCs) may be indicators of population state as their secretion to chronic stress can impair survival and reproduction. However, the relationship between GC secretion, climate change and population extinction risk remains unclear. In this study, we investigated whether levels of baseline corticosterone (the main GCs in reptiles) correlate with environmental conditions and associated extinction risk across wild populations of the common lizard Zootoca vivipara. First, we performed a cross‐sectional comparison of baseline corticosterone levels along an altitudinal gradient among 14 populations. Then, we used a longitudinal study in eight populations to examine the changes in corticosterone levels following the exposure to a heatwave period. Unexpectedly, baseline corticosterone decreased with increasing thermal conditions at rest in females and was not correlated with extinction risk. In addition, baseline corticosterone levels decreased after exposure to an extreme heatwave period. This seasonal corticosterone decrease was more pronounced in populations without access to standing water. We suggest that low basal secretion of corticosterone may entail downregulating activity levels and limit exposure to adverse climatic conditions, especially to reduce water loss. These new insights suggest that rapid population decline might be preceded by a downregulation of the corticosterone secretion

Data from: Reduction of baseline corticosterone secretion correlates with climate warming and drying across wild lizard populations

1. Climate change should lead to massive loss of biodiversity in most taxa but the detailed physiological mechanisms underlying population extinction remain largely elusive so far. In vertebrates, baseline levels of hormones such as glucocorticoids (GCs) may be indicators of population state since their secretion to chronic stress can impair survival and reproduction. However, the relationship between GC secretion, climate change and population extinction risk remains unclear. 2. In this study we investigated whether levels of baseline corticosterone (the main GCs in reptiles) correlate with environmental conditions and associated extinction risk across wild populations of the common lizard Zootoca vivipara. 3. First, we performed a cross-sectional comparison of baseline corticosterone levels along an altitudinal gradient among 14 populations. Then, we used a longitudinal study in 8 populations to examine the changes in corticosterone levels following the exposure to a heat wave period. 4. Unexpectedly, baseline corticosterone decreased with increasing thermal conditions at rest in females, and was not correlated with extinction risk. In addition, baseline corticosterone levels decreased after exposure to an extreme heat wave period. This seasonal corticosterone decrease was more pronounced in populations without access to standing water. 5. We suggest that low basal secretion of corticosterone may entail down-regulating activity levels and limit exposure to adverse climatic conditions, especially to reduce water loss. These new insights suggest that rapid population decline might be preceded by a down-regulation of the corticosterone secretion

Water availability and temperature induce changes in oxidative status during pregnancy in a viviparous lizard

International audienceReproduction involves considerable reorganization in an organism's physiology that incurs potential toxicity for cells (e.g., oxidative stress) and decrease in fitness. This framework has been the cornerstone of the so‐called ‘oxidative cost of reproduction’, a theory that remains controversial and relatively overlooked in non‐model ectotherms. Here, we used two complementary approaches in natural and controlled conditions to test whether altered access to climate conditions (water and temperature resources) alters oxidative status and mediates reproductive trade‐offs in viviparous populations of the common lizard (Zootoca vivipara). First, we examined whether access to free‐standing water and differences in ambient temperature across 12 natural populations could be related to variation in oxidative status, reproductive effort and reproductive success. Second, we determined whether an experimental restriction to water triggers higher oxidative cost of reproduction and correlates with fitness measures (reproductive success, future survival rate and probability of future reproduction). Pregnant females exhibited higher sensitivity than males to natural or experimental limitations in temperature and water access. That is, in restricted environments, pregnant females with higher reproductive effort exhibited stronger oxidative damage despite enhanced non‐enzymatic antioxidant capacity. Enhanced antioxidant defensive capacity in pregnant females was positively correlated with higher reproductive success, whereas elevated oxidative damage negatively correlated with offspring annual survival. Altogether, our results revealed a context‐dependent oxidative cost of reproduction that was concomitant with a conflict in water demand from offspring. These new insights should be critical for understanding ectotherm responses to heat waves and summer droughts that are increasing in frequency and duration

Environmental conditions and male quality traits simultaneously explain variation of multiple colour signals in male lizards

enThis link goes to a English sectionfrThis link goes to a French section Male lizards often display multiple pigment-based and structural colour signals which may reflect various quality traits (e.g. performance, parasitism), with testosterone (T) often mediating these relationships. Furthermore, environmental conditions can explain colour signal variation by affecting processes such as signal efficacy, thermoregulation and camouflage. The relationships between colour signals, male quality traits and environmental factors have often been analysed in isolation, but simultaneous analyses are rare. Thus, the response of multiple colour signals to variation in all these factors in an integrative analysis remains to be investigated. Here, we investigated how multiple colour signals relate to their information content, examined the role of T as a potential mediator of these relationships and how environmental factors explain colour signal variation. We performed an integrative study to examine the covariation between three colour signals (melanin-based black, carotenoid-based yellow–orange and structural UV), physiological performance, parasitism, T levels and environmental factors (microclimate, forest cover) in male common lizards Zootoca vivipara from 13 populations. We found that the three colour signals conveyed information on different aspects of male condition, supporting a multiple message hypothesis. T influenced only parasitism, suggesting that T does not directly mediate the relationships between colour signals and their information content. Moreover, colour signals became more saturated in forested habitats, suggesting an adaptation to degraded light conditions, and became generally brighter in mesic conditions, in contradiction with the thermal melanism hypothesis. We show that distinct individual quality traits and environmental factors simultaneously explain variations of multiple colour signals with different production modes. Our study therefore highlights the complexity of colour signal evolution, involving various sets of selective pressures acting at the same time, but in different ways depending on colour production mechanism