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.

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'.

Evolutionary ecology of dispersal in biodiverse spatially structured systems: what is old and what is new?

Dispersal is a well-recognized driver of ecological and evolutionary dynamics, and simultaneously an evolving trait. Dispersal evolution has traditionally been studied in single-species metapopulations so that it remains unclear how dispersal evolves in metacommunities and metafoodwebs, which are characterized by a multitude of species interactions. Since most natural systems are both species-rich and spatially structured, this knowledge gap should be bridged. Here, we discuss whether knowledge from dispersal evolutionary ecology established in single-species systems holds in metacommunities and metafoodwebs and we highlight generally valid and fundamental principles. Most biotic interactions form the backdrop to the ecological theatre for the evolutionary dispersal play because interactions mediate patterns of fitness expectations across space and time. While this allows for a simple transposition of certain known principles to a multispecies context, other drivers may require more complex transpositions, or might not be transferred. We discuss an important quantitative modulator of dispersal evolution-increased trait dimensionality of biodiverse meta-systems-and an additional driver: co-dispersal. We speculate that scale and selection pressure mismatches owing to co-dispersal, together with increased trait dimensionality, may lead to a slower and more 'diffuse' evolution in biodiverse meta-systems. Open questions and potential consequences in both ecological and evolutionary terms call for more investigation. This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

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 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.

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.

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.

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.

Evolutionary Dynamics of Wild Populations.

Wild populations are facing rapid and sometimes extreme environmental changes that are currently exacerbated by pressing human activities [...].

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.

Congruent Genetic and Demographic Dispersal Rates in a Natural Metapopulation at Equilibrium.

Understanding the functioning of natural metapopulations at relevant spatial and temporal scales is necessary to accurately feed both theoretical eco-evolutionary models and conservation plans. One key metric to describe the dynamics of metapopulations is dispersal rate. It can be estimated with either direct field estimates of individual movements or with indirect molecular methods, but the two approaches do not necessarily match. We present a field study in a large natural metapopulation of the butterfly Boloria eunomia in Belgium surveyed over three generations using synchronized demographic and genetic datasets with the aim to characterize its genetic structure, its dispersal dynamics, and its demographic stability. By comparing the census and effective population sizes, and the estimates of dispersal rates, we found evidence of stability at several levels: constant inter-generational ranking of population sizes without drastic historical changes, stable genetic structure and geographically-influenced dispersal movements. Interestingly, contemporary dispersal estimates matched between direct field and indirect genetic assessments. We discuss the eco-evolutionary mechanisms that could explain the described stability of the metapopulation, and suggest that destabilizing agents like inter-generational fluctuations in population sizes could be controlled by a long adaptive history of the species to its dynamic local environment. We finally propose methodological avenues to further improve the match between demographic and genetic estimates of dispersal.

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.

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.

A User-Centered design and usability testing of a web-based medication reconciliation application integrated in an eHealth network.

BACKGROUND: Medication discrepancies, which are a threat to patient safety, can be reduced by medication reconciliation (MedRec). MedRec is a complex process that can be supported by the use of information technology and patient engagement. Therefore, the SEAMPAT project aims to develop a MedRec IT platform based on two applications. The application for the professionals is called: the "MedRec app". OBJECTIVE: In the present study, we aimed to describe the development and usability testing of the MedRec app, reporting results of a three iterations user-centered usability evaluation. METHODS: We used a three phase iterative user-centered study spread over 16 months. At each phase, the usability evaluation included several methods (observations, questionnaires, and follow-up discussions with participants) to collect quantitative and qualitative data in order to improve the current prototype and evolve to the next prototype. RESULTS: In total, 48 healthcare professionals (25 general practitioners and 23 hospital clinicians) participated to the MedRec app evaluation. There were 14, 32 and 5 participants for phases 1, 2 and 3 respectively. At each phase, many design modifications were done to strengthen usability. Concerning usability, participants considered the prototypes as an acceptable interface with a median System Usability Score of 73 at phase 2 and 75 at phase 3. Participants emphasized the need for improvements concerning workflow integration, usefulness and interoperability. CONCLUSION: The MedRec app was perceived as being useful, usable and satisfying. However, further improvements are required in several usability aspects. Our study demonstrates the importance of conducting usability assessments before investing time and resources in a large study evaluating the effect of an eMedRec approach on clinical outcomes. Our findings may also increase the chances of acceptability and sustained use over time by clinicians.

Mobility affects copulation and oviposition dynamics in Pieris brassicae in seminatural cages.

When, how often and for how long organisms mate can have strong consequences for individual fitness and are crucial aspects of evolutionary ecology. Such determinants are likely to be of even greater importance in monandrous species and species with short adult life stages. Previous work suggests that mobility, a key dispersal-related trait, may affect the dynamics of copulations, but few studies have investigated the impact of individual mobility on mating latency, copulation duration and oviposition latency simultaneously. In this paper, we monitored the copulation dynamics of 40 males and 40 females, as well as the oviposition dynamics of the females of the Large White butterfly Pieris brassicae, a facultative long-distance disperser butterfly. Individuals from a breeding were selected to create a uniform distribution of mobility and we recorded the timing, number and duration of all copulations in a semiexperimental system. We showed that mobility, measured as the time spent in flight under stressful conditions (a proxy of dispersal tendency), correlates with all aspects of copulation dynamics: mobile males and females mated earlier and for shorter periods than less mobile individuals. In turn, late mating females increased the time between copulation and oviposition. These results feed the previously described mobility syndrome of P. brassicae, involving morphological and physiological characters, with life-history traits. We suggest that the reduction of mating latency and copulation duration has an adaptive value in dispersing individuals, as their life expectancy might be shorter than that of sedentary individuals.

Habitat choice meets thermal specialization: Competition with specialists may drive suboptimal habitat preferences in generalists.

Limited dispersal is classically considered as a prerequisite for ecological specialization to evolve, such that generalists are expected to show greater dispersal propensity compared with specialists. However, when individuals choose habitats that maximize their performance instead of dispersing randomly, theory predicts dispersal with habitat choice to evolve in specialists, while generalists should disperse more randomly. We tested whether habitat choice is associated with thermal niche specialization using microcosms of the ciliate Tetrahymena thermophila, a species that performs active dispersal. We found that thermal specialists preferred optimal habitats as predicted by theory, a link that should make specialists more likely to track suitable conditions under environmental changes than expected under the random dispersal assumption. Surprisingly, generalists also performed habitat choice but with a preference for suboptimal habitats. Since this result challenges current theory, we developed a metapopulation model to understand under which circumstances such a preference for suboptimal habitats should evolve. We showed that competition between generalists and specialists may favor a preference for niche margins in generalists under environmental variability. Our results demonstrate that the behavioral dimension of dispersal-here, habitat choice-fundamentally alters our predictions of how dispersal evolve with niche specialization, making dispersal behaviors crucial for ecological forecasting facing environmental changes.