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.

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.

Pollen dispersal slows geographical range shift and accelerates ecological niche shift under climate change.

Species may survive climate change by migrating to track favorable climates and/or adapting to different climates. Several quantitative genetics models predict that species escaping extinction will change their geographical distribution while keeping the same ecological niche. We introduce pollen dispersal in these models, which affects gene flow but not directly colonization. We show that plant populations may escape extinction because of both spatial range and ecological niche shifts. Exact analytical formulas predict that increasing pollen dispersal distance slows the expected spatial range shift and accelerates the ecological niche shift. There is an optimal distance of pollen dispersal, which maximizes the sustainable rate of climate change. These conclusions hold in simulations relaxing several strong assumptions of our analytical model. Our results imply that, for plants with long distance of pollen dispersal, models assuming niche conservatism may not accurately predict their future distribution under climate change.

How Ecology and Landscape Dynamics Shape Phylogenetic Trees.

Whether biotic or abiotic factors are the dominant drivers of clade diversification is a long-standing question in evolutionary biology. The ubiquitous patterns of phylogenetic imbalance and branching slowdown have been taken as supporting the role of ecological niche filling and spatial heterogeneity in ecological features, and thus of biotic processes, in diversification. However, a proper theoretical assessment of the relative roles of biotic and abiotic factors in macroevolution requires models that integrate both types of factors, and such models have been lacking. In this study, we use an individual-based model to investigate the temporal patterns of diversification driven by ecological speciation in a stochastically fluctuating geographic landscape. The model generates phylogenies whose shape evolves as the clade ages. Stabilization of tree shape often occurs after ecological saturation, revealing species turnover caused by competition and demographic stochasticity. In the initial phase of diversification (allopatric radiation into an empty landscape), trees tend to be unbalanced and branching slows down. As diversification proceeds further due to landscape dynamics, balance and branching tempo may increase and become positive. Three main conclusions follow. First, the phylogenies of ecologically saturated clades do not always exhibit branching slowdown. Branching slowdown requires that competition be wide or heterogeneous across the landscape, or that the characteristics of landscape dynamics vary geographically. Conversely, branching acceleration is predicted under narrow competition or frequent local catastrophes. Second, ecological heterogeneity does not necessarily cause phylogenies to be unbalanced--short time in geographical isolation or frequent local catastrophes may lead to balanced trees despite spatial heterogeneity. Conversely, unbalanced trees can emerge without spatial heterogeneity, notably if competition is wide. Third, short isolation time causes a radically different and quite robust pattern of phylogenies that are balanced and yet exhibit branching slowdown. In conclusion, biotic factors have a strong and diverse influence on the shape of phylogenies of ecologically saturating clades and create the evolutionary template in which branching slowdown and tree imbalance may occur. However, the contingency of landscape dynamics and resource distribution can cause wide variation in branching tempo and tree balance. Finally, considerable variation in tree shape among simulation replicates calls for caution when interpreting variation in the shape of real phylogenies.

Islands as model systems in ecology and evolution: prospects fifty years after MacArthur-Wilson.

The study of islands as model systems has played an important role in the development of evolutionary and ecological theory. The 50th anniversary of MacArthur and Wilson's (December 1963) article, 'An equilibrium theory of insular zoogeography', was a recent milestone for this theme. Since 1963, island systems have provided new insights into the formation of ecological communities. Here, building on such developments, we highlight prospects for research on islands to improve our understanding of the ecology and evolution of communities in general. Throughout, we emphasise how attributes of islands combine to provide unusual research opportunities, the implications of which stretch far beyond islands. Molecular tools and increasing data acquisition now permit re-assessment of some fundamental issues that interested MacArthur and Wilson. These include the formation of ecological networks, species abundance distributions, and the contribution of evolution to community assembly. We also extend our prospects to other fields of ecology and evolution - understanding ecosystem functioning, speciation and diversification - frequently employing assets of oceanic islands in inferring the geographic area within which evolution has occurred, and potential barriers to gene flow. Although island-based theory is continually being enriched, incorporating non-equilibrium dynamics is identified as a major challenge for the future.

Dispersal evolution and resource matching in a spatially and temporally variable environment.

Metapopulations may consist of patches of different quality, and are often disturbed by extrinsic processes causing variation of patch quality. The persistence of such metapopulations then depends on the species' dispersal strategy. In a temporally constant environment, the evolution of dispersal rates follows the resource matching rule, i.e. at the evolutionarily stable dispersal strategy the number of competitors in each patch matches the resource availability in each patch. Here, we investigate how the distribution of individuals resulting from convergence stable dispersal strategies would match the distribution of resources in an environment which is temporally variable due to extrinsic disturbance. We develop an analytically tractable asexual model with two qualities of patches. We show that convergence stable dispersal rates are such that resource matching is predicted in expectation before habitat quality variation, and that the distribution of individuals undermatches resources after habitat quality variation. The overall flow of individuals between patches matches the overall flow of resources between patches resulting from environmental variation. We show that these conclusions can be generalized to organisms with sexual reproduction, and to a metapopulation with three qualities of patches when there is no mutational correlation between dispersal rates.

Integrative Phylogenetics: Tools for Palaeontologists to Explore the Tree of Life.

The modern era of analytical and quantitative palaeobiology has only just begun, integrating methods such as morphological and molecular phylogenetics and divergence time estimation, as well as phenotypic and molecular rates of evolution. Calibrating the tree of life to geological time is at the nexus of many disparate disciplines, from palaeontology to molecular systematics and from geochronology to comparative genomics. Creating an evolutionary time scale of the major events that shaped biodiversity is key to all of these fields and draws from each of them. Different methodological approaches and data employed in various disciplines have traditionally made collaborative research efforts difficult among these disciplines. However, the development of new methods is bridging the historical gap between fields, providing a holistic perspective on organismal evolutionary history, integrating all of the available evidence from living and fossil species. Because phylogenies with only extant taxa do not contain enough information to either calibrate the tree of life or fully infer macroevolutionary dynamics, phylogenies should preferably include both extant and extinct taxa, which can only be achieved through the inclusion of phenotypic data. This integrative phylogenetic approach provides ample and novel opportunities for evolutionary biologists to benefit from palaeontological data to help establish an evolutionary time scale and to test core macroevolutionary hypotheses about the drivers of biological diversification across various dimensions of organisms.

Allele fixation in a dynamic metapopulation: founder effects vs refuge effects.

The fixation of mutant alleles has been studied with models assuming various spatial population structures. In these models, the structure of the metapopulation that we call the "landscape" (number, size and connectivity of subpopulations) is often static. However, natural populations are subject to repetitive population size variations, fragmentation and secondary contacts at different spatiotemporal scales due to geological, climatic and ecological processes. In this paper, we examine how such dynamic landscapes can alter mutant fixation probability and time to fixation. We consider three stochastic landscape dynamics: (i) the population is subject to repetitive bottlenecks, (ii) to the repeated alternation of fragmentation and fusion of demes with a constant population carrying capacity, (iii) idem with a variable carrying capacity. We show by deriving a variance, a coalescent and a harmonic mean population effective size, and with simulations that these landscape dynamics generate repetitive founder effects which counteract selection, thereby decreasing the fixation probability of an advantageous mutant but accelerate fixation when it occurs. For models (ii) and (iii), we also highlight an antagonistic "refuge effect" which can strongly delay mutant fixation. The predominance of either founder effects or refuge effects determines the time to fixation and mainly depends on the characteristic time scales of the landscape dynamics.

Male mating constraints affect mutual mate choice: prudent male courting and sperm-limited females.

Costs of sperm production may lead to prudence in male sperm allocation and also to male mate choice. Here, we develop a life history-based mutual mate choice model that takes into account the lost-opportunity costs for males from time out in sperm recovery and lets mate competition be determined by the prevailing mate choice strategies. We assume that high mating rate may potentially lead to sperm depletion in males, and that as a result, female reproduction may be limited by the availability of sperm. Increasing variation in male quality leads, in general, to increased selective mate choice by females, and vice versa. Lower-quality males may, however, gain access to more fecund higher-quality females by lowering their courting rate, thus increasing their sperm reserves. When faced with strong male competition for mates, low-quality males become less choosy, which leads to assortative mating for quality and an increased mating rate across all males. With assortative mating, the frequency of antagonistic interactions (sexual conflict) is reduced, allowing males to lower the time spent replenishing sperm reserves in order to increase mating rate. This in turn leads to lower sperm levels at mating and therefore could lead to negative effects on female fitness via sperm limitation.

Clade diversification dynamics and the biotic and abiotic controls of speciation and extinction rates.

How ecological interactions, genetic processes, and environmental variability jointly shape the evolution of species diversity remains a challenging problem in biology. We developed an individual-based model of clade diversification to predict macroevolutionary dynamics when resource competition, genetic differentiation, and landscape fluctuations interact. Diversification begins with a phase of geographic adaptive radiation. Extinction rates rise sharply at the onset of the next phase. In this phase of niche self-structuring, speciation and extinction processes, albeit driven by biotic mechanisms (competition and hybridization), have essentially constant rates, determined primarily by the abiotic pace of landscape dynamics. The final phase of diversification begins when intense competition prevents dispersing individuals from establishing new populations. Species' ranges shrink, causing negative diversity-dependence of speciation rates. These results show how ecological and microevolutionary processes shape macroevolutionary dynamics and rates; they caution against the notion of ecological limits to diversity, and suggest new directions for the phylogenetic analysis of diversification.

Adaptive radiation driven by the interplay of eco-evolutionary and landscape dynamics.

We investigate an individual-based model of adaptive radiation based on the biogeographical changes of the Great African Lakes where cichlid fishes radiated. In our model, the landscape consists of a mosaic of three habitat types which may or may not be separated by geographic barriers. We study the effect of the alternation between allopatry and sympatry called landscape dynamics. We show that landscape dynamics can generate a significantly higher diversity than allopatric or sympatric speciation alone. Diversification is mainly due to the joint action of allopatric, ecological divergence, and of disruptive selection increasing assortative mating and allowing for the coexistence in sympatry of species following reinforcement or character displacement. Landscape dynamics possibly increase diversity at each landscape change. The characteristics of the radiation depend on the speed of landscape dynamics and of the number of geographically isolated regions at steady state. Under fast dynamics of a landscape with many fragments, the model predicts a high diversity, possibly subject to the temporary collapse of all species into a hybrid swarm. When fast landscape dynamics induce the recurrent fusion of several sites, diversity is moderate but very stable over time. Under slow landscape dynamics, diversification proceeds similarly, although at a slower pace.

The probability of evolutionary rescue: towards a quantitative comparison between theory and evolution experiments.

Evolutionary rescue occurs when a population genetically adapts to a new stressful environment that would otherwise cause its extinction. Forecasting the probability of persistence under stress, including emergence of drug resistance as a special case of interest, requires experimentally validated quantitative predictions. Here, we propose general analytical predictions, based on diffusion approximations, for the probability of evolutionary rescue. We assume a narrow genetic basis for adaptation to stress, as is often the case for drug resistance. First, we extend the rescue model of Orr & Unckless (Am. Nat. 2008 172, 160-169) to a broader demographic and genetic context, allowing the model to apply to empirical systems with variation among mutation effects on demography, overlapping generations and bottlenecks, all common features of microbial populations. Second, we confront our predictions of rescue probability with two datasets from experiments with Saccharomyces cerevisiae (yeast) and Pseudomonas fluorescens (bacterium). The tests show the qualitative agreement between the model and observed patterns, and illustrate how biologically relevant quantities, such as the per capita rate of rescue, can be estimated from fits of empirical data. Finally, we use the results of the model to suggest further, more quantitative, tests of evolutionary rescue theory.

How does pollen versus seed dispersal affect niche evolution?

In heterogeneous landscapes, the genetic and demographic consequences of dispersal influence the evolution of niche width. Unless pollen is limiting, pollen dispersal does not contribute directly to population growth. However, by disrupting local adaptation, it indirectly affects population dynamics. We compare the effect of pollen versus seed dispersal on the evolution of niche width in heterogeneous habitats, explicitly considering the feedback between maladaptation and demography. We consider two scenarios: the secondary contact of two subpopulations, in distinct, formerly isolated habitats, and the colonization of an empty habitat with dispersal between the new and ancestral habitat. With an analytical model, we identify critical levels of genetic variance leading to niche contraction (secondary contact scenario), or expansion (new habitat scenario). We confront these predictions with simulations where the genetic variance freely evolves. Niche contraction occurs when habitats are very different. It is faster as total gene flow increases or as pollen predominates in overall gene flow. Niche expansion occurs when habitat heterogeneity is not too high. Seed dispersal accelerates it, whereas pollen dispersal tends to retard it. In both scenarios very high seed dispersal leads to extinction. Overall, our results predict a wider niche for species dispersing seeds more than pollen.

Under which conditions is character displacement a likely outcome of secondary contact?

Sympatric character displacement is one possible mechanism that prevents competitive exclusion. This mechanism is thought to be behind the radiation of Darwin's finches, where character displacement is assumed to have followed secondary contact of ecologically similar species. We use a model to evaluate under which ecological and environmental conditions this mechanism is likely. Using the adaptive dynamics theory, we analyse different ecological models embedded in the secondary contact scenario. We highlight two necessary conditions for character displacement in sympatry: (i) very strong premating isolation between the two populations, and (ii) secondary contact to occur at an evolutionary branching point. Character displacement is then driven by adaptation to interspecific competition. We determine how ecological and environmental parameters influence the probability of ecological divergence. Finally, we discuss the likelihood of sympatric character displacement under disruptive selection in natural populations.