Warming effects on lizard gut microbiome depend on habitat connectivity.

Climate warming and landscape fragmentation are both factors well known to threaten biodiversity and to generate species responses and adaptation. However, the impact of warming and fragmentation interplay on organismal responses remains largely under-explored, especially when it comes to gut symbionts, which may play a key role in essential host functions and traits by extending its functional and genetic repertoire. Here, we experimentally examined the combined effects of climate warming and habitat connectivity on the gut bacterial communities of the common lizard (Zootoca vivipara) over three years. While the strength of effects varied over the years, we found that a 2°C warmer climate decreases lizard gut microbiome diversity in isolated habitats. However, enabling connectivity among habitats with warmer and cooler climates offset or even reversed warming effects. The warming effects and the association between host dispersal behaviour and microbiome diversity appear to be a potential driver of this interplay. This study suggests that preserving habitat connectivity will play a key role in mitigating climate change impacts, including the diversity of the gut microbiome, and calls for more studies combining multiple anthropogenic stressors when predicting the persistence of species and communities through global changes.

When and how can we predict adaptive responses to climate change?

Predicting if, when, and how populations can adapt to climate change constitutes one of the greatest challenges in science today. Here, we build from contributions to the special issue on evolutionary adaptation to climate change, a survey of its authors, and recent literature to explore the limits and opportunities for predicting adaptive responses to climate change. We outline what might be predictable now, in the future, and perhaps never even with our best efforts. More accurate predictions are expected for traits characterized by a well-understood mapping between genotypes and phenotypes and traits experiencing strong, direct selection due to climate change. A meta-analysis revealed an overall moderate trait heritability and evolvability in studies performed under future climate conditions but indicated no significant change between current and future climate conditions, suggesting neither more nor less genetic variation for adapting to future climates. Predicting population persistence and evolutionary rescue remains uncertain, especially for the many species without sufficient ecological data. Still, when polled, authors contributing to this special issue were relatively optimistic about our ability to predict future evolutionary responses to climate change. Predictions will improve as we expand efforts to understand diverse organisms, their ecology, and their adaptive potential. Advancements in functional genomic resources, especially their extension to non-model species and the union of evolutionary experiments and "omics," should also enhance predictions. Although predicting evolutionary responses to climate change remains challenging, even small advances will reduce the substantial uncertainties surrounding future evolutionary responses to climate change.

Thermal mismatches explain consumer-resource dynamics in response to environmental warming.

Changing temperatures will impact food webs in ways we yet to fully understand. The thermal sensitivities of various physiological and ecological processes differ across organisms and study systems, hindering the generation of accurate predictions. One step towards improving this picture is to acquire a mechanistic understanding of how temperature change impacts trophic interactions before we can scale these insights up to food webs and ecosystems. Here, we implement a mechanistic approach centered on the thermal sensitivity of energetic balances in pairwise consumer-resource interactions, measuring the thermal dependence of energetic gain and loss for two resource and one consumer freshwater species. Quantifying the balance between energy gain and loss, we determined the temperature ranges where the balance decreased for each species in isolation (intraspecific thermal mismatch) and where a mismatch in the balance between consumer and resource species emerged (interspecific thermal mismatch). The latter reveals the temperatures for which consumer and resource energetic balances respond either differently or in the same way, which in turn informs us of the strength of top-down control. We found that warming improved the energetic balance for both resources, but reduces it for the consumer, due to the stronger thermal sensitivity of respiration compared to ingestion. The interspecific thermal mismatch yielded different patterns between the two consumer-resource pairs. In one case, the consumer-resource energetic balance became weaker throughout the temperature gradient, and in the other case it produced a U-shaped response. By also measuring interaction strength for these interaction pairs, we demonstrated the correspondence of interspecific thermal mismatches and interaction strength. Our approach accounts for the energetic traits of both consumer and resource species, which combined produce a good indication of the thermal sensitivity of interaction strength. Thus, this novel approach links thermal ecology with parameters typically explored in food-web studies.

Plastic responses to warmer climates: a semi-natural experiment on lizard populations.

Facing warming environments, species can exhibit plastic or microevolutionary changes in their thermal physiology to adapt to novel climates. Here, using semi-natural mesocosms, we experimentally investigated over two successive years whether a 2°C-warmer climate produces selective and inter- and intragenerational plastic changes in the thermal traits (preferred temperature and dorsal coloration) of the lizard Zootoca vivipara. In a warmer climate, the dorsal darkness, dorsal contrast, and preferred temperature of adults plastically decreased and covariances between these traits were disrupted. While selection gradients were overall weak, selection gradients for darkness were slightly different between climates and in the opposite direction to plastic changes. Contrary to adults, male juveniles were darker in warmer climates either through plasticity or selection and this effect was strengthened by intergenerational plasticity when juveniles' mothers also experienced warmer climates. While the plastic changes in adult thermal traits alleviate the immediate overheating costs of warming, its opposite direction to selective gradients and to juveniles' phenotypic responses may slow down evolutionary shifts toward phenotypes that are better adapted to future climates. Our study demonstrates the importance of considering inter- and intragenerational plasticity along with selective processes to better understand adaptation and population dynamics in light of climate change.

Investigating the genetic basis of vertebrate dispersal combining RNA-seq, RAD-seq and quantitative genetics.

Although animal dispersal is known to play key roles in ecological and evolutionary processes such as colonization, population extinction and local adaptation, little is known about its genetic basis, particularly in vertebrates. Untapping the genetic basis of dispersal should deepen our understanding of how dispersal behaviour evolves, the molecular mechanisms that regulate it and link it to other phenotypic aspects in order to form the so-called dispersal syndromes. Here, we comprehensively combined quantitative genetics, genome-wide sequencing and transcriptome sequencing to investigate the genetic basis of natal dispersal in a known ecological and evolutionary model of vertebrate dispersal: the common lizard, Zootoca vivipara. Our study supports the heritability of dispersal in semi-natural populations, with less variation attributable to maternal and natal environment effects. In addition, we found an association between natal dispersal and both variation in the carbonic anhydrase (CA10) gene, and in the expression of several genes (TGFB2, SLC6A4, NOS1) involved in central nervous system functioning. These findings suggest that neurotransmitters (serotonin and nitric oxide) are involved in the regulation of dispersal and shaping dispersal syndromes. Several genes from the circadian clock (CRY2, KCTD21) were also differentially expressed between disperser and resident lizards, supporting that the circadian rhythm, known to be involved in long-distance migration in other taxa, might affect dispersal as well. Since neuronal and circadian pathways are relatively well conserved across vertebrates, our results are likely to be generalisable, and we therefore encourage future studies to further investigate the role of these pathways in shaping dispersal in vertebrates.

Adaptive Maternal Effects Shape Offspring Phenotype and Survival in Natal Environments.

AbstractMaternal effects can give newborns a head start in life by adjusting natal phenotypes to natal environments, yet their strength and adaptiveness are often difficult to investigate in natural populations. Here, we studied anticipatory maternal effects and their adaptiveness in common lizards in a seminatural experimental system. Specifically, we investigated how maternal environments (i.e., vegetation cover) and maternal phenotype (i.e., activity levels and body length) can shape offspring phenotype. We further studied whether such maternal effects influenced offspring survival in natal environments varying with respect to vegetation cover, conspecific density, and, consequently, maternal fitness. More active females from dense vegetation habitats produced bigger offspring than their less active counterparts, the contrary being true for sparse vegetation habitats. Moreover, females from dense vegetation habitats produced more active offspring and more active offspring survived better in dense vegetation habitats, resulting in greater maternal fitness through maternal effects. These results suggest adaptive anticipatory maternal effects, induced by vegetation structure and mediated by activity levels that may shape early-life prospects in natal environments.

Connectivity among thermal habitats buffers the effects of warm climate on life-history traits and population dynamics.

Contemporary climate change affects population dynamics, but its influence varies with landscape structure. It is still unclear whether landscape fragmentation buffers or amplifies the effects of climate on population size and the age and body size of individuals composing these populations. This study aims to investigate the impacts of warm climates on lizard life-history traits and population dynamics in habitats that vary in their connectivity. We monitored common lizard Zootoca vivipara populations for 3 years in an experimental system in which both climatic conditions and connectivity among habitats were simultaneously manipulated. We considered two climatic treatments (i.e. present-day climate and warm climate [+1.4°C than present-day climate]) and two connectivity treatments (i.e. a connected treatment in which individuals could move from one climate to the other and an isolated treatment in which movement between climates was not possible). We monitored survival, reproduction, growth, dispersal, age and body size of each individual in the system as well as population density through time. We found that the influence of warm climates on life-history traits and population dynamics depended on connectivity among thermal habitats. Populations in warm climates were (i) composed of younger individuals only when isolated; (ii) larger in population size only in connected habitats and (iii) composed of larger age-specific individuals independently of the landscape configuration. The connectivity among habitats altered population responses to climate warming likely through asymmetries in the flow and phenotype of dispersers between thermal habitats. Our results demonstrate that landscape fragmentation can drastically change the dynamics and persistence of populations facing climate change.

Le changement climatique actuel impacte la dynamique des populations, mais son influence varie avec la structure du paysage. A ce jour, il est difficile de prédire si la fragmentation du paysage réduit ou augmente les effets du réchauffement climatique sur la taille des populations, ainsi que sur l'âge et la taille corporelle des individus qui composent ces populations. Cette étude s'intéresse aux impacts d'un climat plus chaud sur les traits d'histoire de vie et la dynamique de populations vivant dans des habitats qui diffèrent quant à leur niveau de connectivité. Pendant trois ans, nous avons suivi des populations de lézards vivipares Zootoca vivipara au sein d'un dispositif expérimental qui permet de manipuler simultanément les conditions climatiques et le niveau de connectivité entre habitats. Nous avons considéré deux traitements climatiques [i.e., climat actuel et climat chaud (+1.4°C plus chaud que le climat actuel)] et deux traitements de connectivité (i.e., un traitement connecté au sein duquel les individus pouvaient se déplacer d'un climat à un autre, et un traitement isolé au sein duquel les déplacements entre climats n'étaient pas permis). Tout au long de l'expérience, nous avons mesuré la survie, la reproduction, la croissance, la dispersion, l'âge et la taille corporelle de chaque individu ainsi que la densité des populations. Nous avons observé que l'influence du climat chaud sur les traits d'histoire de vie et la dynamique de population dépendait du niveau de connectivité entre habitats. Les populations en climat chaud étaient composées (i) d'individus plus jeunes seulement en habitat isolé, (ii) de plus d'individus uniquement en habitat connecté et (iii) d'individus plus grands à âge égal et ce indépendamment de la configuration du paysage. Nos résultats montrent que le niveau de connectivité entre habitats altère les réponses des populations au réchauffement climatique via une asymétrie dans le flux et le phénotype des dispersants entre climats. Nos résultats démontrent que la fragmentation du paysage peut influencer de façon drastique la dynamique et la persistance des populations face au changement climatique.

Dispersal syndromes can link intraspecific trait variability and meta-ecosystem functioning.

Dispersal mediates the flow of organisms in meta-communities and subsequently energy and material flows in meta-ecosystems. Individuals within species often vary in dispersal tendency depending on their phenotypic traits (i.e., dispersal syndromes), but the implications of dispersal syndromes for meta-ecosystems have been rarely studied. Using empirical examples on vertebrates, arthropods, and microbes, we highlight that key functional traits can be linked to dispersal. We argue that this coupling between dispersal and functional traits can have consequences for meta-ecosystem functioning, mediating flows of functional traits and thus the spatial heterogeneity of ecosystem functions. As dispersal syndromes may be genetically determined, the spatial heterogeneity of functional traits may be further carried over across generations and link meta-ecosystem functioning to evolutionary dynamics.

Phytoplankton biodiversity is more important for ecosystem functioning in highly variable thermal environments.

The 21st century has seen an acceleration of anthropogenic climate change and biodiversity loss, with both stressors deemed to affect ecosystem functioning. However, we know little about the interactive effects of both stressors and in particular about the interaction of increased climatic variability and biodiversity loss on ecosystem functioning. This should be remedied because larger climatic variability is one of the main features of climate change. Here, we demonstrated that temperature fluctuations led to changes in the importance of biodiversity for ecosystem functioning. We used microcosm communities of different phytoplankton species richness and exposed them to a constant, mild, and severe temperature-fluctuating environment. Wider temperature fluctuations led to steeper biodiversity-ecosystem functioning slopes, meaning that species loss had a stronger negative effect on ecosystem functioning in more fluctuating environments. For severe temperature fluctuations, the slope increased through time due to a decrease of the productivity of species-poor communities over time. We developed a theoretical competition model to better understand our experimental results and showed that larger differences in thermal tolerances across species led to steeper biodiversity-ecosystem functioning slopes. Species-rich communities maintained their ecosystem functioning with increased fluctuation as they contained species able to resist the thermally fluctuating environments, while this was on average not the case in species-poor communities. Our results highlight the importance of biodiversity for maintaining ecosystem functions and services in the context of increased climatic variability under climate change.

Abrupt declines in marine phytoplankton production driven by warming and biodiversity loss in a microcosm experiment.

Rising sea surface temperatures are expected to lead to the loss of phytoplankton biodiversity. However, we currently understand very little about the interactions between warming, loss of phytoplankton diversity and its impact on the oceans' primary production. We experimentally manipulated the species richness of marine phytoplankton communities under a range of warming scenarios, and found that ecosystem production declined more abruptly with species loss in communities exposed to higher temperatures. Species contributing positively to ecosystem production in the warmed treatments were those that had the highest optimal temperatures for photosynthesis, implying that the synergistic impacts of warming and biodiversity loss on ecosystem functioning were mediated by thermal trait variability. As species were lost from the communities, the probability of taxa remaining that could tolerate warming diminished, resulting in abrupt declines in ecosystem production. Our results highlight the potential for synergistic effects of warming and biodiversity loss on marine primary production.

Altered trophic interactions in warming climates: consequences for predator diet breadth and fitness.

Species interactions are central in predicting the impairment of biodiversity with climate change. Trophic interactions may be altered through climate-dependent changes in either predator food preferences or prey communities. Yet, climate change impacts on predator diet remain surprisingly poorly understood. We experimentally studied the consequences of 2°C warmer climatic conditions on the trophic niche of a generalist lizard predator. We used a system of semi-natural mesocosms housing a variety of invertebrate species and in which climatic conditions were manipulated. Lizards in warmer climatic conditions ate at a greater predatory to phytophagous invertebrate ratio and had smaller individual dietary breadths. These shifts mainly arose from direct impacts of climate on lizard diets rather than from changes in prey communities. Dietary changes were associated with negative changes in fitness-related traits (body condition, gut microbiota) and survival. We demonstrate that climate change alters trophic interactions through top-predator dietary shifts, which might disrupt eco-evolutionary dynamics.

Habitat fragmentation experiments on arthropods: what to do next?

Habitat fragmentation has the potential to influence ecological and evolutionary dynamics in various ways. Fragmentation experiments explore these multiple influences and the underlying mechanisms. We review experiments used in arthropods and highlight gaps in biological focus, methodology and questions addressed. While the consequences on community structure were often reported, fewer studies focused on ecosystem functions and evolutionary processes, with striking gaps on genetic and eco-evolutionary dynamics. Regarding fragmentation components, matrix quality was often overlooked while inter-patch (and source-patch) distance was the most studied component. The identified gaps outlined our need to study fragmentation at different time-scales, and on teasing apart the respective roles of each fragmentation component on each eco-evolutionary process.

Changes in temperature alter the relationship between biodiversity and ecosystem functioning.

Global warming and the loss of biodiversity through human activities (e.g., land-use change, pollution, invasive species) are two of the most profound threats to the functional integrity of the Earth's ecosystems. These factors are, however, most frequently investigated separately, ignoring the potential for synergistic effects of biodiversity loss and environmental warming on ecosystem functioning. Here we use high-throughput experiments with microbial communities to investigate how changes in temperature affect the relationship between biodiversity and ecosystem functioning. We found that changes in temperature systematically altered the relationship between biodiversity and ecosystem functioning. As temperatures departed from ambient conditions the exponent of the diversity-functioning relationship increased, meaning that more species were required to maintain ecosystem functioning under thermal stress. This key result was driven by two processes linked to variability in the thermal tolerance curves of taxa. First, more diverse communities had a greater chance of including species with thermal traits that enabled them to maintain productivity as temperatures shifted from ambient conditions. Second, we found a pronounced increase in the contribution of complementarity to the net biodiversity effect at high and low temperatures, indicating that changes in species interactions played a critical role in mediating the impacts of temperature change on the relationship between biodiversity and ecosystem functioning. Our results highlight that if biodiversity loss occurs independently of species' thermal tolerance traits, then the additional impacts of environmental warming will result in sharp declines in ecosystem function.

Role of carbon allocation efficiency in the temperature dependence of autotroph growth rates.

Relating the temperature dependence of photosynthetic biomass production to underlying metabolic rates in autotrophs is crucial for predicting the effects of climatic temperature fluctuations on the carbon balance of ecosystems. We present a mathematical model that links thermal performance curves (TPCs) of photosynthesis, respiration, and carbon allocation efficiency to the exponential growth rate of a population of photosynthetic autotroph cells. Using experiments with the green alga, Chlorella vulgaris, we apply the model to show that the temperature dependence of carbon allocation efficiency is key to understanding responses of growth rates to warming at both ecological and longer-term evolutionary timescales. Finally, we assemble a dataset of multiple terrestrial and aquatic autotroph species to show that the effects of temperature-dependent carbon allocation efficiency on potential growth rate TPCs are expected to be consistent across taxa. In particular, both the thermal sensitivity and the optimal temperature of growth rates are expected to change significantly due to temperature dependence of carbon allocation efficiency alone. Our study provides a foundation for understanding how the temperature dependence of carbon allocation determines how population growth rates respond to temperature.

Metabolic traits predict the effects of warming on phytoplankton competition.

Understanding how changes in temperature affect interspecific competition is critical for predicting changes in ecological communities with global warming. Here, we develop a theoretical model that links interspecific differences in the temperature dependence of resource acquisition and growth to the outcome of pairwise competition in phytoplankton. We parameterised our model with these metabolic traits derived from six species of freshwater phytoplankton and tested its ability to predict the outcome of competition in all pairwise combinations of the species in a factorial experiment, manipulating temperature and nutrient availability. The model correctly predicted the outcome of competition in 72% of the pairwise experiments, with competitive advantage determined by difference in thermal sensitivity of growth rates of the two species. These results demonstrate that metabolic traits play a key role in determining how changes in temperature influence interspecific competition and lay the foundation for mechanistically predicting the effects of warming in complex, multi-species communities.

Climate warming reduces gut microbiota diversity in a vertebrate ectotherm.

Climate change is now considered to be the greatest threat to biodiversity and ecological networks, but its impacts on the bacterial communities associated with plants and animals remain largely unknown. Here, we studied the consequences of climate warming on the gut bacterial communities of an ectotherm, the common lizard (Zootoca vivipara), using a semi-natural experimental approach. We found that 2-3 °C warmer climates cause a 34% loss of populations' microbiota diversity, with possible negative consequences for host survival.

Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis.

Phytoplankton photosynthesis is a critical flux in the carbon cycle, accounting for approximately 40% of the carbon dioxide fixed globally on an annual basis and fuelling the productivity of aquatic food webs. However, rapid evolutionary responses of phytoplankton to warming remain largely unexplored, particularly outside the laboratory, where multiple selection pressures can modify adaptation to environmental change. Here, we use a decade-long experiment in outdoor mesocosms to investigate mechanisms of adaptation to warming (+4 °C above ambient temperature) in the green alga Chlamydomonas reinhardtii, in naturally assembled communities. Isolates from warmed mesocosms had higher optimal growth temperatures than their counterparts from ambient treatments. Consequently, warm-adapted isolates were stronger competitors at elevated temperature and experienced a decline in competitive fitness in ambient conditions, indicating adaptation to local thermal regimes. Higher competitive fitness in the warmed isolates was linked to greater photosynthetic capacity and reduced susceptibility to photoinhibition. These findings suggest that adaptive responses to warming in phytoplankton could help to mitigate projected declines in aquatic net primary production by increasing rates of cellular net photosynthesis.

Live Fast, Die Young: Experimental Evidence of Population Extinction Risk due to Climate Change.

Evidence has accumulated in recent decades on the drastic impact of climate change on biodiversity. Warming temperatures have induced changes in species physiology, phenology, and have decreased body size. Such modifications can impact population dynamics and could lead to changes in life cycle and demography. More specifically, conceptual frameworks predict that global warming will severely threaten tropical ectotherms while temperate ectotherms should resist or even benefit from higher temperatures. However, experimental studies measuring the impacts of future warming trends on temperate ectotherms' life cycle and population persistence are lacking. Here we investigate the impacts of future climates on a model vertebrate ectotherm species using a large-scale warming experiment. We manipulated climatic conditions in 18 seminatural populations over two years to obtain a present climate treatment and a warm climate treatment matching IPCC predictions for future climate. Warmer temperatures caused a faster body growth, an earlier reproductive onset, and an increased voltinism, leading to a highly accelerated life cycle but also to a decrease in adult survival. A matrix population model predicts that warm climate populations in our experiment should go extinct in around 20 y. Comparing our experimental climatic conditions to conditions encountered by populations across Europe, we suggest that warming climates should threaten a significant number of populations at the southern range of the distribution. Our findings stress the importance of experimental approaches on the entire life cycle to more accurately predict population and species persistence in future climates.

Maternal exposure to predator scents: offspring phenotypic adjustment and dispersal.

Predation is a strong selective pressure generating morphological, physiological and behavioural responses in organisms. As predation risk is often higher during juvenile stages, antipredator defences expressed early in life are paramount to survival. Maternal effects are an efficient pathway to produce such defences. We investigated whether maternal exposure to predator cues during gestation affected juvenile morphology, behaviour and dispersal in common lizards (Zootoca vivipara). We exposed 21 gravid females to saurophagous snake cues for one month while 21 females remained unexposed (i.e. control). We measured body size, preferred temperature and activity level for each neonate, and released them into semi-natural enclosures connected to corridors in order to measure dispersal. Offspring from exposed mothers grew longer tails, selected lower temperatures and dispersed thrice more than offspring from unexposed mothers. Because both tail autotomy and altered thermoregulatory behaviour are common antipredator tactics in lizards, these results suggest that mothers adjusted offspring phenotype to risky natal environments (tail length) or increased risk avoidance (dispersal). Although maternal effects can be passive consequences of maternal stress, our results strongly militate for them to be an adaptive antipredator response that may increase offspring survival prospects.