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.

Ecological responses of squamate reptiles to nocturnal warming.

Nocturnal temperatures are increasing at a pace exceeding diurnal temperatures in most parts of the world. The role of warmer nocturnal temperatures in animal ecology has received scant attention and most studies focus on diurnal or daily descriptors of thermal environments' temporal trends. Yet, available evidence from plant and insect studies suggests that organisms can exhibit contrasting physiological responses to diurnal and nocturnal warming. Limiting studies to diurnal trends can thus result in incomplete and misleading interpretations of the ability of species to cope with global warming. Although they are expected to be impacted by warmer nocturnal temperatures, insufficient data are available regarding the night-time ecology of vertebrate ectotherms. Here, we illustrate the complex effects of nocturnal warming on squamate reptiles, a keystone group of vertebrate ectotherms. Our review includes discussion of diurnal and nocturnal ectotherms, but we mainly focus on diurnal species for which nocturnal warming affects a period dedicated to physiological recovery, and thus may perturb activity patterns and energy balance. We first summarise the physical consequences of nocturnal warming on habitats used by squamate reptiles. Second, we describe how such changes can alter the energy balance of diurnal species. We illustrate this with empirical data from the asp viper (Vipera aspis) and common wall lizard (Podarcis muralis), two diurnal species found throughout western Europe. Third, we make use of a mechanistic approach based on an energy-balance model to draw general conclusions about the effects of nocturnal temperatures. Fourth, we examine how warmer nights may affect squamates over their lifetime, with potential consequences on individual fitness and population dynamics. We review quantitative evidence for such lifetime effects using recent data derived from a range of studies on the European common lizard (Zootoca vivipara). Finally, we consider the broader eco-evolutionary ramifications of nocturnal warming and highlight several research questions that require future attention. Our work emphasises the importance of considering the joint influence of diurnal and nocturnal warming on the responses of vertebrate ectotherms to climate warming.

Stage dependence of phenotypical and phenological maternal effects: insight into squamate reptile reproductive strategies.

Enhanced thermal conditions have been credited as a driving force for the evolution of viviparity, particularly in squamate reptiles, among which it has independently evolved more than 100 times. However, maternal thermoregulation is also a critical component of reproduction in oviparous squamates, for which considerable embryonic development occurs prior to oviposition. When carrying eggs, oviparous mothers modify thermoregulation in a manner similar to that of pregnant females. To further understand the role of temperature in influencing reproductive strategies, it is critical that we elucidate the degree to which thermal sensitivity varies across developmental stages. We studied stage-dependent embryonic sensitivity in a viviparous snake, the aspic viper (Vipera aspis). We manipulated female body temperature at different stages of pregnancy-early development, early embryonic growth, and late embryonic growth-by imposing two contrasting daily thermal cycles that mimicked reproductive (warm) and nonreproductive (cool) female temperature profiles. Thermal sensitivity of offspring phenotype was stage dependent, with offspring quality more negatively affected when exposure to cool temperatures occurred early in development. In contrast, developmental rate was slowed by the cooler cycle, independent of the timing of the exposure. Given the more persistent effect on phenology, phenological effects likely provide a greater driving force for complete embryonic retention (i.e., viviparity).

What drives the risk of being bitten by a viper? A fine spatial scale study in western France.

Previous studies on viper bites in France have focused on clinical consequences of envenomation, efficacy of antivenom and epidemiology of bites. Herein, we wanted to clarify temporal and spatial patterns in bite incidence using a fine spatial scale (municipality level). We focused on viper bites recorded over the last 10 years in 4 regions of western France. We addressed the determinants of bite occurrence and number of bites considering the following variables: predicted probability of viper presence, species (V. aspis or V. berus), climatic data, tourism function rate, soil transformation and landscape use. 703 bite cases were retained with significant disparities between areas. Bites occurred either during a garden-related activity (339 cases, 51.2%) or during an activity in the countryside (300 cases, 45.3%). The probability of presence of a viper at the municipality level positively influenced the risk of being bitten (multiplied by 3 for a variation in probability of 0.25 from 0.5) but varied between species (lower in V. berus than V. aspis). Artificial land development had a positive effect on bite risks. Finally, a tourism function rate above 50 beds/100 inhabitants was strongly associated with an increase in the risk of occurrence and frequency of bites. Overall, viper bites recorded in our study were concentrated on the south coastline of Pays de la Loire region. The coastal towns are significant areas of tourist attraction and are located close to preserved semi-natural landscapes that provide favorable habitats for vipers. This convergence may favor human/wildlife encounters.

Water deprivation compromises maternal physiology and reproductive success in a cold and wet adapted snake Vipera berus.

Droughts are becoming more intense and frequent with climate change. These extreme weather events can lead to mass mortality and reproduction failure, and therefore cause population declines. Understanding how the reproductive physiology of organisms is affected by water shortages will help clarify whether females can adjust their reproductive strategy to dry conditions or may fail to reproduce and survive. In this study, we investigated the consequences of a short period of water deprivation (2 weeks) during early pregnancy on the physiology and behaviour of a cold- and wet-adapted ectotherm (Vipera berus). We also examined water allocation to developing embryos and embryonic survival. Water-deprived females exhibited significant dehydration, physiological stress and loss of muscle mass. These effects of water deprivation on water balance and muscle loss were correlated with the number of developing embryos. While water-deprived females maintained water transfer to embryos at the expense of their own maintenance, water deprivation also led to embryonic mortality. Overall, water deprivation amplifies the reproductive costs of water allocation to support embryonic development. The deleterious impacts of water deprivation on female current reproductive performance and on potential survival and future reproduction could lead to severe population declines in this species.

Hydric "Costs" of Reproduction: Pregnancy Increases Evaporative Water Loss in the Snake Vipera aspis.

Water constraints can mediate evolutionary conflict either among individuals (e.g., parent-offspring conflict, sexual conflict) or within an individual (e.g., cost of reproduction). During pregnancy, water is of particular importance because the female provides all water needed for embryonic development and experiences important maternal shifts in behavior and physiology that, together, can compromise female water balance if water availability is limited. We examined the effect of pregnancy on evaporative water loss and microhabitat selection in a viviparous snake, the aspic viper. We found that both physiological (increased metabolism and body temperature) and morphological (body distension) changes contribute to an increased evaporative water loss in pregnant females. We also found that pregnant females in the wild select warmer and moister basking locations than nonreproductive females, likely to mitigate the conflict between thermal needs and water loss. Water resources likely induce significant reproductive constraints across diverse taxa and thus warrant further consideration in ecological research. From an evolutionary perspective, water constraints during reproduction may contribute to shaping reproductive effort.

Cold climate specialization: adaptive covariation between metabolic rate and thermoregulation in pregnant vipers.

We compared thermoregulatory strategies during pregnancy in two congeneric viperid snakes (Vipera berus and Vipera aspis) with parapatric geographic ranges. V. berus is a boreal specialist with the largest known distribution among terrestrial snakes while V. aspis is a south-European species. Despite contrasted climatic affinities, the two species displayed identical thermal preferences (Tset) in a laboratory thermal gradient. Under identical natural conditions, however, V. berus was capable of maintaining Tset for longer periods, especially when the weather was constraining. Consistent with the metabolic cold adaptation hypothesis, V. berus displayed higher standard metabolic rate at all temperatures considered. We used the thermal dependence of metabolic rate to calculate daily metabolic profiles from body temperature under natural conditions. The boreal specialist experienced higher daily metabolic rate and minimized gestation duration chiefly because of differences in the metabolic reaction norms, but also superior thermoregulatory efficiency. Under cold climates, thermal constraints should make precise thermoregulation costly. However, a shift in the metabolic reaction norm may compensate for thermal constraints and modify the cost-benefit balance of thermoregulation. Covariation between metabolic rate and thermoregulation efficiency is likely an important adaptation to cold climates.