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.

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.

Dispersal syndromes in challenging environments: A cross-species experiment.

Dispersal is a central biological process tightly integrated into life-histories, morphology, physiology and behaviour. Such associations, or syndromes, are anticipated to impact the eco-evolutionary dynamics of spatially structured populations, and cascade into ecosystem processes. As for dispersal on its own, these syndromes are likely neither fixed nor random, but conditional on the experienced environment. We experimentally studied how dispersal propensity varies with individuals' phenotype and local environmental harshness using 15 species ranging from protists to vertebrates. We reveal a general phenotypic dispersal syndrome across studied species, with dispersers being larger, more active and having a marked locomotion-oriented morphology and a strengthening of the link between dispersal and some phenotypic traits with environmental harshness. Our proof-of-concept metacommunity model further reveals cascading effects of context-dependent syndromes on the local and regional organisation of functional diversity. Our study opens new avenues to advance our understanding of the functioning of spatially structured populations, communities and ecosystems.

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.

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.

Reproductive fitness consequences of progenesis: Sex-specific pay-offs in safe and risky environments.

Progenesis is considered to have an important role in evolution because it allows the retention of both a larval body size and shape in an adult morphology. However, the cost caused by the adoption of a progenetic process in both males and females remains to be explored to explain the success of progenesis and particularly its biased prevalence across the sexes and environments. Here, through an experimental approach, we used a facultative progenetic species, the palmate newt (Lissotriton helveticus) that can either mature at a small size and retain gills or mature after metamorphosis, to test three hypotheses for sex-specific pay-offs of progenesis in safe versus risky habitats. Goldfish were used because they caused a higher decline in progenetic than metamorphic newts. We determined that progenetic newts have a lower reproductive fitness than metamorphic newts. We also found that, when compared to metamorphs, progenetic males have lower reproductive activity than progenetic females and that predatory risk affects more progenetic than metamorphic newts. By identifying ultimate causes of the female-biased sex ratios found in nature, these results support the male escape hypothesis, that is the higher metamorphosis rate of progenetic males. They also highlight that although progenesis is advantageous in advancing the age at first reproduction, it also brings an immediate fitness cost and this, particularly, in hostile predatory environments. This means that whereas some environmental constraints could favour facultative progenesis, some others, such as predation, can ultimately counter-select progenesis. Altogether, these results improve our understanding of how developmental processes can affect the sexes differently and how species invasions can impair the success of alternative developmental phenotypes.

Bottom-up and top-down control of dispersal across major organismal groups.

Ecology and evolution unfold in spatially structured communities, where dispersal links dynamics across scales. Because dispersal is multicausal, identifying general drivers remains challenging. In a coordinated distributed experiment spanning organisms from protozoa to vertebrates, we tested whether two fundamental determinants of local dynamics, top-down and bottom-up control, generally explain active dispersal. We show that both factors consistently increased emigration rates and use metacommunity modelling to highlight consequences on local and regional dynamics.

Integrating Ecological and Evolutionary Context in the Study of Maternal Stress.

Maternal stress can prenatally influence offspring phenotypes and there are an increasing number of ecological studies that are bringing to bear biomedical findings to natural systems. This is resulting in a shift from the perspective that maternal stress is unanimously costly, to one in which maternal stress may be beneficial to offspring. However, this adaptive perspective is in its infancy with much progress to still be made in understanding the role of maternal stress in natural systems. Our aim is to emphasize the importance of the ecological and evolutionary context within which adaptive hypotheses of maternal stress can be evaluated. We present five primary research areas where we think future research can make substantial progress: (1) understanding maternal and offspring control mechanisms that modulate exposure between maternal stress and subsequent offspring phenotype response; (2) understanding the dynamic nature of the interaction between mothers and their environment; (3) integrating offspring phenotypic responses and measuring both maternal and offspring fitness outcomes under real-life (either free-living or semi-natural) conditions; (4) empirically testing these fitness outcomes across relevant spatial and temporal environmental contexts (both pre- and post-natal environments); (5) examining the role of maternal stress effects in human-altered environments-i.e., do they limit or enhance fitness. To make progress, it is critical to understand the role of maternal stress in an ecological context and to do that, we must integrate across physiology, behavior, genetics, and evolution.

Introduced goldfish affect amphibians through inhibition of sexual behaviour in risky habitats: an experimental approach.

The introduction of alien species is one of the major causes of current and global biodiversity loss. The introduction of fish can be a particular threat to native amphibian populations, which are declining worldwide. One way for amphibians to persist in such altered environments is to adopt anti-predator strategies especially at the behavioural level. However, although it has been shown that avoidance behaviour may decrease the probability of being detected by a potential predator, little is known on the consequences on sexual behaviour. In this study, we tested the hypothesis that adult Alpine newts (Ichthyosaura alpestris) use shelters more often and exhibit less sexual activity in the presence of goldfish (Carassius auratus) and that they reduce sexual activity more in risky micro-habitats than in safe environments. To this end, we assessed behavioural patterns of adult newts in a replicated laboratory design. Goldfish were present in direct contact with newts in half of the tanks. Consistently throughout the study period, significantly more newts used shelter in the presence of fish than in their absence. Newts also significantly decreased their sexual activity level overall, but specially outside the shelter when they were in direct contact with fish. These results show that fish presence can affect newts in complex ways, such as through inhibition of their reproduction. Our work highlights that integrating behaviour in conservation studies is essential to understanding the patterns of coexistence and exclusion between introduced fish and amphibians.

The use of visual and automatized behavioral markers to assess methodologies: a study case on PIT-tagging in the Alpine newt.

In various research fields, biomarkers are now widely used as tools for assessing individual integrity. The recent advances in quantification methods for behavioral patterns, such as computerized video-tracking procedures, make them valuable biomarkers. However, the corollary of these novelties is that they remain relatively unknown and unused. In this study, we show that such tools can assess the validity of research methods, such as individual recognition. To demonstrate this, we employed, as a model, a marking method (passive integrated transponder [PIT] tagging) widely used in amphibians. Detailed visual observations and video-tracking methods were complementary in highlighting components at different behavioral scales: locomotion, feeding, and breeding. We illustrate the scientific and ethical adequacy of the targeted marking method but also suggest that more studies should integrate behavioral analyses. Such biomarkers are a powerful tool for assessing conservation concerns when other techniques cannot detect detrimental effects.