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.

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.

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 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 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.

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.

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.

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.

Short Physical Performance Battery and all-cause mortality: systematic review and meta-analysis.

BACKGROUND: The Short Physical Performance Battery (SPPB) is a well-established tool to assess lower extremity physical performance status. Its predictive ability for all-cause mortality has been sparsely reported, but with conflicting results in different subsets of participants. The aim of this study was to perform a meta-analysis investigating the relationship between SPPB score and all-cause mortality. METHODS: Articles were searched in MEDLINE, the Cochrane Library, Google Scholar, and BioMed Central between July and September 2015 and updated in January 2016. Inclusion criteria were observational studies; >50 participants; stratification of population according to SPPB value; data on all-cause mortality; English language publications. Twenty-four articles were selected from available evidence. Data of interest (i.e., clinical characteristics, information after stratification of the sample into four SPPB groups [0-3, 4-6, 7-9, 10-12]) were retrieved from the articles and/or obtained by the study authors. The odds ratio (OR) and/or hazard ratio (HR) was obtained for all-cause mortality according to SPPB category (with SPPB scores 10-12 considered as reference) with adjustment for age, sex, and body mass index. RESULTS: Standardized data were obtained for 17 studies (n = 16,534, mean age 76 ± 3 years). As compared to SPPB scores 10-12, values of 0-3 (OR 3.25, 95%CI 2.86-3.79), 4-6 (OR 2.14, 95%CI 1.92-2.39), and 7-9 (OR 1.50, 95%CI 1.32-1.71) were each associated with an increased risk of all-cause mortality. The association between poor performance on SPPB and all-cause mortality remained highly consistent independent of follow-up length, subsets of participants, geographic area, and age of the population. Random effects meta-regression showed that OR for all-cause mortality with SPPB values 7-9 was higher in the younger population, diabetics, and men. CONCLUSIONS: An SPPB score lower than 10 is predictive of all-cause mortality. The systematic implementation of the SPPB in clinical practice settings may provide useful prognostic information about the risk of all-cause mortality. Moreover, the SPPB could be used as a surrogate endpoint of all-cause mortality in trials needing to quantify benefit and health improvements of specific treatments or rehabilitation programs. The study protocol was published on PROSPERO (CRD42015024916).

Evolution of a butterfly dispersal syndrome.

The existence of dispersal syndromes contrasting disperser from resident phenotypes within populations has been intensively documented across taxa. However, how such suites of phenotypic traits emerge and are maintained is largely unknown, although deciphering the processes shaping the evolution of dispersal phenotypes is a key in ecology and evolution. In this study, we created artificial populations of a butterfly, in which we controlled for individual phenotypes and measured experimentally the roles of selection and genetic constraints on the correlations between dispersal-related traits: flight performance and wing morphology. We demonstrate that (i) trait covariations are not due to genetic correlations, (ii) the effects of selection are sex-specific, and (iii) both divergent and stabilizing selection maintain specific flight performance phenotypes and wing morphologies. Interestingly, some trait combinations are also favoured, depending on sex and fitness components. Moreover, we provide evidence for the role of (dis)assortative mating in the evolution of these dispersal-related traits. Our results suggest that dispersal syndromes may have high evolutionary potential, but also that they may be easily disrupted under particular environmental conditions.

The Metatron: an experimental system to study dispersal and metaecosystems for terrestrial organisms.

Dispersal of organisms generates gene flow between populations. Identifying factors that influence dispersal will help predict how species will cope with rapid environmental change. We developed an innovative infrastructure, the Metatron, composed of 48 interconnected patches, designed for the study of terrestrial organism movement as a model for dispersal. Corridors between patches can be flexibly open or closed. Temperature, humidity and illuminance can be independently controlled within each patch. The modularity and adaptability of the Metatron provide the opportunity for robust experimental design for the study of 'meta-systems'. We describe a pilot experiment on populations of the butterfly Pieris brassicae and the lizard Zootoca vivipara in the Metatron. Both species survived and showed both disperser and resident phenotypes. The Metatron offers the opportunity to test theoretical models in spatial ecology.

The STIB score: a simple clinical test to predict clopidogrel resistance.

BACKGROUND: High platelet reactivity (HPR) to clopidogrel is associated with an increased risk of ischaemic complications during and after coronary interventions and concerns up to 50% of patients undergoing PCI. AIM OF THE STUDY: The aim of the study was to identify patients with HPR to clopidogrel using bedside clinical information obtained in the Stent Thrombosis In Belgium (STIB) trial. METHODS: Data on platelet reactivity using the VerifyNow® point-of-care assay were obtained in 844 patients undergoing PCI for stable coronary artery disease 12 to 24 hours after a 600-mg loading dose of clopidogrel was given. Demographic, clinical and baseline routine biological tests were obtained and compared with P2Y12 reaction units (PRU). Patients with PRU>230 (HPR) were considered as non-responders to clopidogrel. RESULTS: HPR was observed in 424/844 pts. Age, weight, body mass index (BMI), HPR to aspirin, diabetes, renal failure (MDRD<60 ml/min), haemoglobin (Hb), haematocrit, fibrinogen, glycaemia and glycated haemoglobin were associated with HPR to clopidogrel. In multivariate analysis, only Hb (OR: 0.77), BMI (OR: 1.06) and diabetes (OR: 1.62) emerged as independent risk factors. Hb<13.9 g/dl, BMI>28 kg/m2 and presence of diabetes were equally associated to predict HPR and can be added to derive a simple score to predict clopidogrel resistance. Although 38.5% of patients without a single clinical predictor still have HPR, 2/3 patients with 2 or 3 risk factors are resistant to clopidogrel. CONCLUSIONS: STIB HPR score allows identification of patients with a high probability of resistance to clopidogrel based on diabetes, Hb<13.9 g/dl and BMI>28 kg/m2. This bedside clinical test could be useful for the identification of patients in whom another P2Y12 inhibitor should be recommended before and after PCI.

Distinguishing migration from isolation using genes with intragenic recombination: detecting introgression in the Drosophila simulans species complex.

BACKGROUND: Determining the presence or absence of gene flow between populations is the target of some statistical methods in population genetics. Until recently, these methods either avoided the use of recombining genes, or treated recombination as a nuisance parameter. However, genes with recombination contribute additional information for the detection of gene flow (i.e. through linkage disequilibrium). METHODS: We present three summary statistics based on the spatial arrangement of fixed differences, and shared and exclusive polymorphisms that are sensitive to the presence and direction of gene flow. Power and false positive rate for tests based on these statistics are studied by simulation. RESULTS: The application of these tests to populations from the Drosophila simulans species complex yielded results consistent with migration between D. simulans and its two endemic sister species D. mauritiana and D. sechellia, and between populations D. mauritiana on the islands of the Mauritius and Rodrigues. CONCLUSIONS: We demonstrate the sensitivity of the developed statistics to the presence and direction of gene flow, and characterize their power as a function of differentiation level and recombination rate. The properties of these statistics make them especially suitable for analyzing high-throughput sequencing data or for their integration within the approximate Bayesian computation framework.

The glomerular filtration rate estimated by new and old equations as a predictor of important outcomes in elderly patients.

BACKGROUND: The prevalence of chronic kidney disease (CKD) increases with age, and new glomerular filtration rate-estimating equations have recently been validated. The epidemiology of CKD in older individuals and the relationship between a low estimated glomerular filtration rate as calculated by these equations and adverse outcomes remains unknown. METHODS: Data from the BELFRAIL study, a prospective, population-based cohort study of 539 individuals aged 80 years and older, were used. For every participant, five equations were used to calculate estimated glomerular filtration rate based on serum creatinine and/or cystatin C values: MDRD, CKD-EPIcreat, CKD-EPIcyst, CKD-EPIcreatcyst, and BIS equations. The outcomes analyzed included mortality combined with the necessity of new renal replacement therapy, severe cardiovascular events, and hospitalization. RESULTS: During the follow-up period, which was an average of 2.9 years, 124 participants died, 7 required renal replacement therapy, 271 were hospitalized, and 73 had a severe cardiovascular event. The prevalence of estimated glomerular filtration rate values <60 mL/min/1.73 m2 differed depending on the equation used as follows: 44% (MDRD), 45% (CKD-EPIcreat), 75% (CKD-EPIcyst), 65% (CKD-EPIcreatcyst), and 80% (BIS). All of the glomerular filtration rate-estimating equations revealed that higher cardiovascular mortality was associated with lower estimated glomerular filtration rates and that higher probabilities of hospitalization were associated with estimated glomerular filtration rates <30 mL/min/1.73 m2. A lower estimated glomerular filtration rate did not predict a higher probability of severe cardiovascular events, except when using the CKD-EPIcyst equation. By calculating the net reclassification improvement, CKD-EPIcyst and CKD-EPIcreatcyst were shown to predict mortality (+25% and +18%) and severe cardiovascular events (+7% and +9%) with the highest accuracy. The BIS equation was less accurate in predicting mortality (-12%). CONCLUSION: Higher prevalence of CKD were found using the CKD-EPIcyst, CKD-EPIcreatcyst, and BIS equations compared with the MDRD and CKD-EPIcreat equations. The new CKD-EPIcreatcyst and CKD-EPIcyst equations appear to be better predictors of mortality and severe cardiovascular events.

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.

The phenotypic and demographic response to the combination of copper and thermal stressors strongly varies within the ciliate species, Tetrahymena thermophila.

Copper pollution can alter biological and trophic functions. Organisms can utilise different tolerance strategies, including accumulation mechanisms (intracellular vacuoles, external chelation, etc.) to maintain themselves in copper-polluted environments. Accumulation mechanisms can influence the expression of other phenotypic traits, allowing organisms to deal with copper stress. Whether copper effects on accumulation strategies interact with other environmental stressors such as temperature and how this may differ within species are still unsolved questions. Here, we tested experimentally whether the combined effect of copper and temperature modulates traits linked to demography, morphology, movement and accumulation in six strains of the ciliate Tetrahymena thermophila. We also explored whether copper accumulation might modulate environmental copper concentration effects on phenotypic and demographic traits. Results showed high intraspecific variability in the phenotypic and demographic response to copper, with interactive effects between temperature and copper. In addition, they suggested an attenuation effect of copper accumulation on the sensitivity of traits to copper, but with great variation between strains, temperatures and copper concentrations. Diversity of responses among strains and their thermal dependencies pleads for the integration of intraspecific variability and multiple stressors approaches in ecotoxicological studies, thus improving the reliability of assessments of the effects of pollutants on biodiversity.

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'.

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.

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'.