Microbiota and the Volatile Profile of Avian Nests Associate with Each Other and with the Intensity of Parasitism.

Bacteria have been suggested as being partially responsible for avian-nest odours and, thus, volatiles from their metabolism could influence the intensity of selection pressures due to parasites detecting olfactory cues of their hosts. Here, we tested this hypothesis by exploring intra- and interspecific variability in microbial environments, volatile profiles, and intensity of ectoparasitism by Carnus hemapterus in nests of ten avian species. As expected, we found that (i) alpha and beta diversity of microbial and volatile profiles associated to each other. Moreover, (ii) alpha diversity of bacteria and volatiles of nest environment, as well as some particular bacteria and volatiles, associated with intensity of parasitism at early and late stage of the nestling period. Finally, (iii) alpha diversity of the nest microbiota, as well as some particular bacteria and volatiles, was correlated to fledging success. When considering them together, the results support the expected links between microbial environment and nest odours in different bird species, and between microbial environment and both ectoparasitism intensity and fledging success. Relative abundances of particular volatiles and bacteria predicted ectoparasitism and/or fledging success. Future research should prioritize experimental approaches directed to determine the role of bacteria and volatiles in the outcomes of host-ectoparasite interactions.

Species interactions affect dispersal: a meta-analysis.

Context-dependent dispersal allows organisms to seek and settle in habitats improving their fitness. Despite the importance of species interactions in determining fitness, a quantitative synthesis of how they affect dispersal is lacking. We present a meta-analysis asking (i) whether the interaction experienced and/or perceived by a focal species (detrimental interaction with predators, competitors, parasites or beneficial interaction with resources, hosts, mutualists) affects its dispersal; and (ii) how the species' ecological and biological background affects the direction and strength of this interaction-dependent dispersal. After a systematic search focusing on actively dispersing species, we extracted 397 effect sizes from 118 empirical studies encompassing 221 species pairs; arthropods were best represented, followed by vertebrates, protists and others. Detrimental species interactions increased the focal species' dispersal (adjusted effect: 0.33 [0.06, 0.60]), while beneficial interactions decreased it (-0.55 [-0.92, -0.17]). The effect depended on the dispersal phase, with detrimental interactors having opposite impacts on emigration and transience. Interaction-dependent dispersal was negatively related to species' interaction strength, and depended on the global community composition, with cues of presence having stronger effects than the presence of the interactor and the ecological complexity of the community. Our work demonstrates the importance of interspecific interactions on dispersal plasticity, with consequences for metacommunity dynamics.This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

The interplay between abiotic and biotic factors in dispersal decisions in metacommunities.

Suitable conditions for species to survive and reproduce constitute their ecological niche, which is built by abiotic conditions and interactions with conspecifics and heterospecifics. Organisms should ideally assess and use information about all these environmental dimensions to adjust their dispersal decisions depending on their own internal conditions. Dispersal plasticity is often considered through its dependence on abiotic conditions or conspecific density and, to a lesser extent, with reference to the effects of interactions with heterospecifics, potentially leading to misinterpretation of dispersal drivers. Here, we first review the evidence for the effects of and the potential interplays between abiotic factors, biotic interactions with conspecifics and heterospecifics and phenotype on dispersal decisions. We then present an experimental test of these potential interplays, investigating the effects of density and interactions with conspecifics and heterospecifics on temperature-dependent dispersal in microcosms of Tetrahymena ciliates. We found significant differences in dispersal rates depending on the temperature, density and presence of another strain or species. However, the presence and density of conspecifics and heterospecifics had no effects on the thermal-dependency of dispersal. We discuss the causes and consequences of the (lack of) interplay between the different environmental dimensions and the phenotype for metacommunity assembly and dynamics. This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

Phenotypic plasticity and the effects of thermal fluctuations on specialists and generalists.

Classical theories predict that relatively constant environments should generally favour specialists, while fluctuating environments should be selected for generalists. However, theoretical and empirical results have pointed out that generalist organisms might, on the contrary, perform poorly under fluctuations. In particular, if generalism is underlaid by phenotypic plasticity, performance of generalists should be modulated by the temporal characteristics of environmental fluctuations. Here, we used experiments in microcosms of Tetrahymena thermophila ciliates and a mathematical model to test whether the period or autocorrelation of thermal fluctuations mediate links between the level of generalism and the performance of organisms under fluctuations. In the experiment, thermal fluctuations consistently impeded performance compared with constant conditions. However, the intensity of this effect depended on the level of generalism: while the more specialist strains performed better under fast or negatively autocorrelated fluctuations, plastic generalists performed better under slow or positively autocorrelated fluctuations. Our model suggests that these effects of fluctuations on organisms' performance may result from a time delay in the expression of plasticity, restricting its benefits to slow enough fluctuations. This study points out the need to further investigate the temporal dynamics of phenotypic plasticity to better predict its fitness consequences under environmental fluctuations.

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.

Demography and movement patterns of a freshwater ciliate: The influence of oxygen availability.

In freshwater habitats, aerobic animals and microorganisms can react to oxygen deprivation by a series of behavioural and physiological changes, either as a direct consequence of hindered performance or as adaptive responses towards hypoxic conditions. Since oxygen availability can vary throughout the water column, different strategies exist to avoid hypoxia, including that of active 'flight' from low-oxygen sites. Alternatively, some organisms may invest in slower movement, saving energy until conditions return to more favourable levels, which may be described as a 'sit-and-wait' strategy. Here, we aimed to determine which, if any, of these strategies could be used by the freshwater ciliate Tetrahymena thermophila when faced with decreasing levels of oxygen availability in the culture medium. We manipulated oxygen flux into clonal cultures of six strains (i.e. genotypes) and followed their growth kinetics for several weeks using automated image analysis, allowing to precisely quantify changes in density, morphology and movement patterns. Oxygen effects on demography and morphology were comparable across strains: reducing oxygen flux decreased the growth rate and maximal density of experimental cultures, while greatly expanding the duration of their stationary phase. Cells sampled during their exponential growth phase were larger and had a more elongated shape under hypoxic conditions, likely mirroring a shift in resource investment towards individual development rather than frequent divisions. In addition to these general patterns, we found evidence for intraspecific variability in movement responses to oxygen limitation. Some strains showed a reduction in swimming speed, potentially associated with a 'sit-and-wait' strategy; however, the frequent alteration of movement paths towards more linear trajectories also suggests the existence of an inducible 'flight response' in this species. Considering the inherent costs of turns associated with non-linear movement, such a strategy may allow ciliates to escape suboptimal environments at a low energetic cost.

Non-genetic phenotypic variability affects populations and communities in protist microcosms.

Intraspecific trait variation (ITV), potentially driven by genetic and non-genetic mechanisms, can underlie variability in resource acquisition, individual fitness and ecological interactions. Impacts of ITV at higher levels of biological organizations are hence likely, but up-scaling our knowledge about ITV importance to communities and comparing its relative effects at population and community levels has rarely been investigated. Here, we tested the effects of genetic and non-genetic ITV on morphological traits in microcosms of protist communities by contrasting the effects of strains showing different ITV levels (i.e. trait averages and variance) on population growth, community composition and biomass production. We found that genetic and non-genetic ITV can lead to different effects on populations and communities across several generations. Furthermore, the effects of ITV declined across levels of biological organization: ITV directly altered population performance, with cascading but indirect consequences for community composition and biomass productivity. Overall, these results show that the drivers of ITV can have distinct effects on populations and communities, with cascading impacts on higher levels of biological organization that might mediate biodiversity-ecosystem functioning relationships.

The macronuclear genomic landscape within Tetrahymena thermophila.

The extent of intraspecific genomic variation is key to understanding species evolutionary history, including recent adaptive shifts. Intraspecific genomic variation remains poorly explored in eukaryotic micro-organisms, especially in the nuclear dimorphic ciliates, despite their fundamental role as laboratory model systems and their ecological importance in many ecosystems. We sequenced the macronuclear genome of 22 laboratory strains of the oligohymenophoran Tetrahymena thermophila, a model species in both cellular biology and evolutionary ecology. We explored polymorphisms at the junctions of programmed eliminated sequences, and reveal their utility to barcode very closely related cells. As for other species of the genus Tetrahymena, we confirm micronuclear centromeres as gene diversification centres in T. thermophila, but also reveal a two-speed evolution in these regions. In the rest of the genome, we highlight recent diversification of genes coding for extracellular proteins and cell adhesion. We discuss all these findings in relation to this ciliate's ecology and cellular characteristics.

Beyond reaction norms: the temporal dynamics of phenotypic plasticity.

Phenotypic plasticity can allow organisms to cope with environmental changes. Although reaction norms are commonly used to quantify plasticity along gradients of environmental conditions, they often miss the temporal dynamics of phenotypic change, especially the speed at which it occurs. Here, we argue that studying the rate of phenotypic plasticity is a crucial step to quantify and understand its adaptiveness. Iteratively measuring plastic traits allows us to describe the actual dynamics of phenotypic changes and avoid quantifying reaction norms at times that do not truly reflect the organism's capacity for plasticity. Integrating the temporal component in how we describe, quantify, and conceptualise phenotypic plasticity can change our understanding of its diversity, evolution, and consequences.

Resident-Disperser Differences and Genetic Variability Affect Communities in Microcosms.

AbstractDispersal is a key process mediating ecological and evolutionary dynamics. Its effects on the dynamics of spatially structured systems, population genetics, and species range distribution can depend on phenotypic differences between dispersing and nondispersing individuals. However, scaling up the importance of resident-disperser differences to communities and ecosystems has rarely been considered, in spite of intraspecific phenotypic variability being an important factor mediating community structure and productivity. Here, we used the ciliate Tetrahymena thermophila, in which phenotypic traits are known to differ between residents and dispersers, to test (i) whether these resident-disperser differences affect biomass and composition in competitive communities composed of four other Tetrahymena species and (ii) whether these effects are genotype dependent. We found that dispersers led to a lower community biomass compared with residents. This effect was highly consistent across the 20 T. thermophila genotypes used, despite intraspecific variability in resident-disperser phenotypic differences. We also found a significant genotypic effect on biomass production, showing that intraspecific variability has consequences for communities. Our study suggests that individual dispersal strategy can scale up to community productivity in a predictable way, opening new perspectives to the functioning of spatially structured ecosystems.

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.

Dispersal plasticity driven by variation in fitness across species and environmental gradients.

Dispersal plasticity, when organisms adjust their dispersal decisions depending on their environment, can play a major role in ecological and evolutionary dynamics, but how it relates to fitness remains scarcely explored. Theory predicts that high dispersal plasticity should evolve when environmental gradients have a strong impact on fitness. Using microcosms, we tested in five species of the genus Tetrahymena whether dispersal plasticity relates to differences in fitness sensitivity along three environmental gradients. Dispersal plasticity was species- and environment-dependent. As expected, dispersal plasticity was generally related to fitness sensitivity, with higher dispersal plasticity when fitness is more affected by environmental gradients. Individuals often preferentially disperse out of low fitness environments, but leaving environments that should yield high fitness was also commonly observed. We provide empirical support for a fundamental, but largely untested, assumption in dispersal theory: the extent of dispersal plasticity correlates with fitness sensitivity to the environment.

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.

Phenotypic plasticity through disposable genetic adaptation in ciliates.

Ciliates have an extraordinary genetic system in which each cell harbors two distinct kinds of nucleus, a transcriptionally active somatic nucleus and a quiescent germline nucleus. The latter undergoes classical, heritable genetic adaptation, while adaptation of the somatic nucleus is only short-term and thus disposable. The ecological and evolutionary relevance of this nuclear dimorphism have never been well formalized, which is surprising given the long history of using ciliates such as Tetrahymena and Paramecium as model organisms. We present a novel, alternative explanation for ciliate nuclear dimorphism which, we argue, should be considered an instrument of phenotypic plasticity by somatic selection on the level of the ciliate clone, as if it were a diffuse multicellular organism. This viewpoint helps to put some enigmatic aspects of ciliate biology into perspective and presents the diversity of ciliates as a large natural experiment that we can exploit to study phenotypic plasticity and organismality.

Plastic cell morphology changes during dispersal.

Dispersal is the movement of organisms from one habitat to another that potentially results in gene flow. It is often plastic, allowing organisms to adjust dispersal movements depending on environmental conditions. A fundamental aim in ecology is to understand the determinants underlying dispersal and its plasticity. We utilized 22 strains of the ciliate Tetrahymena thermophila to determine if different phenotypic dispersal strategies co-exist within a species and which mechanisms underlie this variability. We quantified the cell morphologies impacting cell motility and dispersal. Distinct differences in innate cellular morphology and dispersal rates were detected, but no universally utilized combinations of morphological parameters correlate with dispersal. Rather, multiple distinct and plastic morphological changes impact cilia-dependent motility during dispersal, especially in proficient dispersing strains facing challenging environmental conditions. Combining ecology and cell biology experiments, we show that dispersal can be promoted through plastic motility-associated changes to cell morphology and motile cilia.

Phenotypic plasticity can reverse the relative extent of intra- and interspecific variability across a thermal gradient.

Intra- and interspecific variability can both ensure ecosystem functions. Generalizing the effects of individual and species assemblages requires understanding how much within and between species trait variation is genetically based or results from phenotypic plasticity. Phenotypic plasticity can indeed lead to rapid and important changes of trait distributions, and in turn community functionality, depending on environmental conditions, which raises a crucial question: could phenotypic plasticity modify the relative importance of intra- and interspecific variability along environmental gradients? We quantified the fundamental niche of five genotypes in monocultures for each of five ciliate species along a wide thermal gradient in standardized conditions to assess the importance of phenotypic plasticity for the level of intraspecific variability compared to differences between species. We showed that phenotypic plasticity strongly influences trait variability and reverses the relative extent of intra- and interspecific variability along the thermal gradient. Our results show that phenotypic plasticity may lead to either increase or decrease of functional trait variability along environmental gradients, making intra- and interspecific variability highly dynamic components of ecological systems.

Fragmentation mediates thermal habitat choice in ciliate microcosms.

Habitat fragmentation is expected to reduce dispersal movements among patches as a result of increased inter-patch distances. Furthermore, since habitat fragmentation is expected to raise the costs of moving among patches in the landscape, it should hamper the ability or tendency of organisms to perform informed dispersal decisions. Here, we used microcosms of the ciliate Tetrahymena thermophila to test experimentally whether habitat fragmentation, manipulated through the length of corridors connecting patches differing in temperature, affects habitat choice. We showed that a twofold increase of inter-patch distance can as expected hamper the ability of organisms to choose their habitat at immigration. Interestingly, it also increased their habitat choice at emigration, suggesting that organisms become choosier in their decision to either stay or leave their patch when obtaining information about neighbouring patches gets harder. This study points out that habitat fragmentation might affect not only dispersal rate but also the level of non-randomness of dispersal, with emigration and immigration decisions differently affected. These consequences of fragmentation might considerably modify ecological and evolutionary dynamics of populations facing environmental changes.

Variability in Dispersal Syndromes Is a Key Driver of Metapopulation Dynamics in Experimental Microcosms.

Evolutionary ecology studies have increasingly focused on the impact of intraspecific variability on population processes. However, the role such variation plays in the dynamics of spatially structured populations and how it interacts with environmental changes remains unclear. Here we experimentally quantify the relative importance of intraspecific variability in dispersal-related traits and spatiotemporal variability of environmental conditions for the dynamics of two-patch metapopulations using clonal genotypes of a ciliate in connected microcosms. We demonstrate that in our simple two-patch microcosms, differences among genotypes are at least as important as spatiotemporal variability of resources for metapopulation dynamics. Furthermore, we show that an important proportion of this effect results from variability of dispersal syndromes. These syndromes can therefore be as important for metapopulation dynamics as spatiotemporal variability of environmental conditions. This study demonstrates that intraspecific variability in dispersal syndromes can be key in the functioning of metapopulations facing environmental changes.

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.