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.

Heat shocks during egg incubation led to developmental, morphological, and behavioral differences in Arctic charr (Salvelinus alpinus).

Temperature variation is affecting fish biodiversity worldwide, causing changes in geographic distribution, phenotypic structure, and even species extinction. Incubation is a critical stage for stenothermic species, which are vulnerable to large temperature fluctuations, and its effects on the phenotype at later developmental stages are understudied, despite the fact that the phenotype being essential for organism ecology and evolution. In this study, we tested the effects of heat shocks during the embryonic period on the phenotype of Arctic charr (Salvelinus alpinus). We repeatedly quantified multiple phenotypic traits, including morphology, development, and behavior, over a period of 4 months, from hatching to juvenile stage in individuals that had experienced heat shocks (+ 5°C on 24 h, seven times) during their embryonic stage and those that had not. We found that heat shocks led to smaller body size at hatching and a lower sociability. Interestingly, these effects weakened throughout the development of individuals and even reversed in the case of body size. We also found an accelerated growth rate and a higher body condition in the presence of heat shocks. Our study provides evidence that heat shocks experienced during incubation can have long-lasting effects on an individual's phenotype. This highlights the importance of the incubation phase for the development of ectothermic organisms and suggests that temperature fluctuations may have significant ecological and evolutionary implications for Arctic charr. Given the predicted increase in extreme events and the unpredictability of temperature fluctuations, it is critical to further investigate their effects on development by examining fluctuations that vary in frequency and intensity.

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.

Genetic erosion reduces biomass temporal stability in wild fish populations.

Genetic diversity sustains species adaptation. However, it may also support key ecosystems functions and services, for example biomass production, that can be altered by the worldwide loss of genetic diversity. Despite extensive experimental evidence, there have been few attempts to empirically test whether genetic diversity actually promotes biomass and biomass stability in wild populations. Here, using long-term demographic wild fish data from two large river basins in southwestern France, we demonstrate through causal modeling analyses that populations with high genetic diversity do not reach higher biomasses than populations with low genetic diversity. Nonetheless, populations with high genetic diversity have much more stable biomasses over recent decades than populations having suffered from genetic erosion, which has implications for the provision of ecosystem services and the risk of population extinction. Our results strengthen the importance of adopting prominent environmental policies to conserve this important biodiversity facet.

Phylogenetically-conserved candidate genes unify biodiversity-ecosystem function relationships and eco-evolutionary dynamics across biological scales.

The intra- and interspecific facets of biodiversity have traditionally been analysed separately, limiting our understanding of how evolution has shaped biodiversity, how biodiversity (as a whole) alters ecological dynamics and hence eco-evolutionary feedbacks at the community scale. Here, we propose using candidate genes phylogenetically-conserved across species and sustaining functional traits as an inclusive biodiversity unit transcending the intra- and interspecific boundaries. This framework merges knowledge from functional genomics and functional ecology, and we first provide guidelines and a concrete example for identifying phylogenetically-conserved candidate genes (PCCGs) within communities and for measuring biodiversity from PCCGs. We then explain how biodiversity measured at PCCGs can be linked to ecosystem functions, which unifies recent observations that both intra- and interspecific biodiversity are important for ecosystem functions. We then highlight the eco-evolutionary processes shaping PCCG diversity patterns and argue that their respective role can be inferred from concepts derived from population genetics. Finally, we explain how PCCGs may shift the field of eco-evolutionary dynamics from a focal-species approach to a more realistic focal-community approach. This framework provides a novel perspective to investigate the global ecosystem consequences of diversity loss across biological scales, and how these ecological changes further alter biodiversity evolution.

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 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.

Intraspecific diversity loss in a predator species alters prey community structure and ecosystem functions.

Loss in intraspecific diversity can alter ecosystem functions, but the underlying mechanisms are still elusive, and intraspecific biodiversity-ecosystem function (iBEF) relationships have been restrained to primary producers. Here, we manipulated genetic and functional richness of a fish consumer (Phoxinus phoxinus) to test whether iBEF relationships exist in consumer species and whether they are more likely sustained by genetic or functional richness. We found that both genotypic and functional richness affected ecosystem functioning, either independently or interactively. Loss in genotypic richness reduced benthic invertebrate diversity consistently across functional richness treatments, whereas it reduced zooplankton diversity only when functional richness was high. Finally, losses in genotypic and functional richness altered functions (decomposition) through trophic cascades. We concluded that iBEF relationships lead to substantial top-down effects on entire food chains. The loss of genotypic richness impacted ecological properties as much as the loss of functional richness, probably because it sustains "cryptic" functional diversity.

Reduction in the metabolic levels due to phenotypic plasticity in the Pyrenean newt, Calotriton asper, during cave colonization.

According to theories on cave adaptation, cave organisms are expected to develop a lower metabolic rate compared to surface organisms as an adaptation to food scarcity in the subterranean environments. To test this hypothesis, we compared the oxygen consumption rates of the surface and subterranean populations of a surface-dwelling species, the newt Calotriton asper, occasionally found in caves. In this study, we designed a new experimental setup in which animals with free movement were monitored for several days in a respirometer. First, we measured the metabolic rates of individuals from the surface and subterranean populations, both maintained for eight years in captivity in a natural cave. We then tested individuals from these populations immediately after they were caught and one year later while being maintained in the cave. We found that the surface individuals that acclimated to the cave significantly reduced their oxygen consumption, whereas individuals from the subterranean population maintained in the cave under a light/dark cycle did not significantly modify their metabolic rates. Second, we compared these metabolic rates to those of an obligate subterranean salamander (Proteus anguinus), a surface aquatic Urodel (Ambystoma mexicanum), and a fish species (Gobio occitaniae) as references for surface organisms from different phyla. As predicted, we found differences between the subterranean and surface species, and the metabolic rates of surface and subterranean C. asper populations were between those of the obligate subterranean and surface species. These results suggest that the plasticity of the metabolism observed in surface C. asper was neither directly due to food availability in our experiments nor the light/dark conditions, but due to static temperatures. Moreover, we suggest that this adjustment of the metabolic level at a temperature close to the thermal optimum may further allow individual species to cope with the food limitations of the subterranean environment.

A river runs through it: The causes, consequences, and management of intraspecific diversity in river networks.

Rivers are fascinating ecosystems in which the eco-evolutionary dynamics of organisms are constrained by particular features, and biologists have developed a wealth of knowledge about freshwater biodiversity patterns. Over the last 10 years, our group used a holistic approach to contribute to this knowledge by focusing on the causes and consequences of intraspecific diversity in rivers. We conducted empirical works on temperate permanent rivers from southern France, and we broadened the scope of our findings using experiments, meta-analyses, and simulations. We demonstrated that intraspecific (genetic) diversity follows a spatial pattern (downstream increase in diversity) that is repeatable across taxa (from plants to vertebrates) and river systems. This pattern can result from interactive processes that we teased apart using appropriate simulation approaches. We further experimentally showed that intraspecific diversity matters for the functioning of river ecosystems. It indeed affects not only community dynamics, but also key ecosystem functions such as litter degradation. This means that losing intraspecific diversity in rivers can yield major ecological effects. Our work on the impact of multiple human stressors on intraspecific diversity revealed that-in the studied river systems-stocking of domestic (fish) strains strongly and consistently alters natural spatial patterns of diversity. It also highlighted the need for specific analytical tools to tease apart spurious from actual relationships in the wild. Finally, we developed original conservation strategies at the basin scale based on the systematic conservation planning framework that appeared pertinent for preserving intraspecific diversity in rivers. We identified several important research avenues that should further facilitate our understanding of patterns of local adaptation in rivers, the identification of processes sustaining intraspecific biodiversity-ecosystem function relationships, and the setting of reliable conservation plans.

Does range expansion modify trait covariation? A study of a northward expanding dragonfly.

The adaptive value of correlations among phenotypic traits depends on the prevailing environmental conditions. Differences in selection pressures during species range expansions may therefore shape phenotypic integration. In this study, we assessed variation in behavioral and morphological traits, as well as their covariations, in replicated southern and northern European populations of the northward expanding dragonfly Crocothemis erythraea. Larvae from northern populations were, on average, darker in color, and therefore, better camouflaged than larvae from southern populations. However, there was no difference in activity level. Darkness and activity were positively correlated in larvae from northern populations, whereas this trait covariation was missing in southern populations. This suggests the emergence of alternative strategies in time-limited northern populations, a higher activity level that required better camouflage through darker coloration, while less active larvae benefited from an energy-saving strategy by reducing the investment in costly traits, such as body darkness. We further found that larger larvae emerged into larger adults, with a higher investment in flight morphology. Our findings imply that phenotypic integration is associated with the northward range shift, potentially differentially shaping fitness consequences, and ecological interactions in southern versus northern populations.

Variability of functional traits and their syndromes in a freshwater fish species (Phoxinus phoxinus): The role of adaptive and nonadaptive processes.

Functional traits can covary to form "functional syndromes." Describing and understanding functional syndromes is an important prerequisite for predicting the effects of organisms on ecosystem functioning. At the intraspecific level, functional syndromes have recently been described, but very little is known about their variability among populations and-if they vary-what the ecological and evolutionary drivers of this variation are. Here, we quantified and compared the variability in four functional traits (body mass, metabolic rate, excretion rate, and boldness), their covariations and the subsequent syndromes among thirteen populations of a common freshwater fish (the European minnow, Phoxinus phoxinus). We then tested whether functional traits and their covariations, as well as the subsequent syndromes, were underpinned by the phylogenetic relatedness among populations (historical effects) or the local environment (i.e., temperature and predation pressure), and whether adaptive (selection or plasticity) or nonadaptive (genetic drift) processes sustained among-population variability. We found substantial among-population variability in functional traits and trait covariations, and in the emerging syndromes. We further found that adaptive mechanisms (plasticity and/or selection) related to water temperature and predation pressure modulated the covariation between body mass and metabolic rate. Other trait covariations were more likely driven by genetic drift, suggesting that nonadaptive processes can also lead to substantial differences in trait covariations among populations. Overall, we concluded that functional syndromes are population-specific, and that both adaptive and nonadaptive processes are shaping functional traits. Given the pivotal role of functional traits, differences in functional syndromes within species provide interesting perspectives regarding the role of intraspecific diversity for ecosystem functioning.

The community and ecosystem consequences of intraspecific diversity: a meta-analysis.

Understanding the relationships between biodiversity and ecosystem functioning has major implications. Biodiversity-ecosystem functioning relationships are generally investigated at the interspecific level, although intraspecific diversity (i.e. within-species diversity) is increasingly perceived as an important ecological facet of biodiversity. Here, we provide a quantitative and integrative synthesis testing, across diverse plant and animal species, whether intraspecific diversity is a major driver of community dynamics and ecosystem functioning. We specifically tested (i) whether the number of genotypes/phenotypes (i.e. intraspecific richness) or the specific identity of genotypes/phenotypes (i.e. intraspecific variation) in populations modulate the structure of communities and the functioning of ecosystems, (ii) whether the ecological effects of intraspecific richness and variation are strong in magnitude, and (iii) whether these effects vary among taxonomic groups and ecological responses. We found a non-linear relationship between intraspecific richness and community and ecosystem dynamics that follows a saturating curve shape, as observed for biodiversity-function relationships measured at the interspecific level. Importantly, intraspecific richness modulated ecological dynamics with a magnitude that was equal to that previously reported for interspecific richness. Our results further confirm, based on a database containing more than 50 species, that intraspecific variation also has substantial effects on ecological dynamics. We demonstrated that the effects of intraspecific variation are twice as high as expected by chance, and that they might have been underestimated previously. Finally, we found that the ecological effects of intraspecific variation are not homogeneous and are actually stronger when intraspecific variation is manipulated in primary producers than in consumer species, and when they are measured at the ecosystem rather than at the community level. Overall, we demonstrated that the two facets of intraspecific diversity (richness and variation) can both strongly affect community and ecosystem dynamics, which reveals the pivotal role of within-species biodiversity for understanding ecological dynamics.

The functional syndrome: linking individual trait variability to ecosystem functioning.

Phenotypic variability is increasingly assessed through functional response and effect traits, which provide a mechanistic framework for investigating how an organism responds to varying ecological factors and how these responses affect ecosystem functioning. Covariation between response and effect traits has been poorly examined at the intraspecific level, thus hampering progress in understanding how phenotypic variability alters the role of organisms in ecosystems. Using a multi-trait approach and a nine-month longitudinal monitoring of individual red-swamp crayfish (Procambarus clarkii), we demonstrated that most of the measured response and effect traits were partially stable during the ontogeny of individuals. Suites of response and effect traits were associated with a response syndrome and an effect syndrome, respectively, which were correlated to form a functional syndrome. Using a bioenergetic model, we predicted that differences in the response syndrome composition of hypothetical populations had important ecological effects on a key ecosystem process (i.e. whole-lake litter decomposition) to a level similar to those induced by doubling population size. Demonstrating the existence of a functional syndrome is likely to improve our understanding of the ecological impacts of phenotypic variation among individuals in wild populations across levels of biological organization, and the linkage between ecosystem and evolutionary ecology.