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'.

Intraspecific demographic and trait responses to environmental change drivers are linked in two species of ciliate.

BACKGROUND: Over the past decade, theory and observations have suggested intraspecific variation, trait-based differences within species, as a buffer against biodiversity loss from multiple environmental changes. This buffering effect can only occur when different populations of the same species respond differently to environmental change. More specifically, variation of demographic responses fosters buffering of demography, while variation of trait responses fosters buffering of functioning. Understanding how both responses are related is important for predicting biodiversity loss and its consequences. In this study, we aimed to empirically assess whether population-level trait responses to multiple environmental change drivers are related to the demographic response to these drivers. To this end, we measured demographic and trait responses in microcosm experiments with two species of ciliated protists. For three clonal strains of each species, we measured responses to two environmental change drivers (climate change and pollution) and their combination. We also examined if relationships between demographic and trait responses existed across treatments and strains. RESULTS: We found different demographic responses across strains of the same species but hardly any interactive effects between the two environmental change drivers. Also, trait responses (summarized in a survival strategy index) varied among strains within a species, again with no driver interactions. Demographic and trait responses were related across all strains of both species tested in this study: Increasing intrinsic growth and self-limitation were associated with a shift in survival strategy from sit-and-wait towards flee. CONCLUSIONS: Our results support the existence of a link between a population's demographic and trait responses to environmental change drivers in two species of ciliate. Future work could dive deeper into the specifics of phenotypical trait values, and changes therein, related to specific life strategies in different species of ciliate and other zooplankton grazers.

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.

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.

Complexity vs linearity: relations between functional traits in a heterotrophic protist.

BACKGROUND: Functional traits are phenotypic traits that affect an organism's performance and shape ecosystem-level processes. The main challenge when using functional traits to quantify biodiversity is to choose which ones to measure since effort and money are limited. As one way of dealing with this, Hodgson et al. (Oikos 85:282, 1999) introduced the idea of two types of traits, with soft traits that are easy and quick to quantify, and hard traits that are directly linked to ecosystem functioning but difficult to measure. If a link exists between the two types of traits, then one could use soft traits as a proxy for hard traits for a quick but meaningful assessment of biodiversity. However, this framework is based on two assumptions: (1) hard and soft traits must be tightly connected to allow reliable prediction of one using the other; (2) the relationship between traits must be monotonic and linear to be detected by the most common statistical techniques (e.g. linear model, PCA). RESULTS: Here we addressed those two assumptions by focusing on six functional traits of the protist species Tetrahymena thermophila, which vary both in their measurement difficulty and functional meaningfulness. They were classified as: easy traits (morphological traits), intermediate traits (movement traits) and hard traits (oxygen consumption and population growth rate). We detected a high number (> 60%) of non-linear relations between the traits, which can explain the low number of significant relations found using linear models and PCA analysis. Overall, these analyses did not detect any relationship strong enough to predict one trait using another, but that does not imply there are none. CONCLUSIONS: Our results highlighted the need to critically assess the relations among the functional traits used as proxies and those functional traits which they aim to reflect. A thorough assessment of whether such relations exist across species and communities is a necessary next step to evaluate whether it is possible to take a shortcut in quantifying functional diversity by collecting the data on easily measurable traits.

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 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.

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.

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.

The interplay between movement, morphology and dispersal in Tetrahymena ciliates.

Understanding how and why individual movement translates into dispersal between populations is a long-term goal in ecology. Movement is broadly defined as 'any change in the spatial location of an individual', whereas dispersal is more narrowly defined as a movement that may lead to gene flow. Because the former may create the condition for the latter, behavioural decisions that lead to dispersal may be detectable in underlying movement behaviour. In addition, dispersing individuals also have specific sets of morphological and behavioural traits that help them coping with the costs of movement and dispersal, and traits that mitigate costs should be under selection and evolve if they have a genetic basis. Here, we experimentally study the relationships between movement behaviour, morphology and dispersal across 44 genotypes of the actively dispersing unicellular, aquatic model organism Tetrahymena thermophila. We used two-patch populations to quantify individual movement trajectories, as well as activity, morphology and dispersal rate. First, we studied variation in movement behaviour among and within genotypes (i.e. between dispersers and residents) and tested whether this variation can be explained by morphology. Then, we addressed how much the dispersal rate is driven by differences in the underlying movement behaviour. Genotypes revealed clear differences in terms of movement speed and linearity. We also detected marked movement differences between resident and dispersing individuals, mediated by the genotype. Movement variation was partly explained by morphological properties such as cell size and shape, with larger cells consistently showing higher movement speed and higher linearity. Genetic differences in activity and movement were positively related to the observed dispersal and jointly explained 47% of the variation in dispersal rate. Our study shows that a detailed understanding of the interplay between morphology, movement and dispersal may have potential to improve dispersal predictions over broader spatio-temporal scales.

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.

Bottom-up and top-down control of dispersal across major organismal groups.

Ecology and evolution unfold in spatially structured communities, where dispersal links dynamics across scales. Because dispersal is multicausal, identifying general drivers remains challenging. In a coordinated distributed experiment spanning organisms from protozoa to vertebrates, we tested whether two fundamental determinants of local dynamics, top-down and bottom-up control, generally explain active dispersal. We show that both factors consistently increased emigration rates and use metacommunity modelling to highlight consequences on local and regional dynamics.

To replicate, or not to replicate - that is the question: how to tackle nonlinear responses in ecological experiments.

A fundamental challenge in experimental ecology is to capture nonlinearities of ecological responses to interacting environmental drivers. Here, we demonstrate that gradient designs outperform replicated designs for detecting and quantifying nonlinear responses. We report the results of (1) multiple computer simulations and (2) two purpose-designed empirical experiments. The findings consistently revealed that unreplicated sampling at a maximum number of sampling locations maximised prediction success (i.e. the R² to the known truth) irrespective of the amount of stochasticity and the underlying response surfaces, including combinations of two linear, unimodal or saturating drivers. For the two empirical experiments, the same pattern was found, with gradient designs outperforming replicated designs in revealing the response surfaces of underlying drivers. Our findings suggest that a move to gradient designs in ecological experiments could be a major step towards unravelling underlying response patterns to continuous and interacting environmental drivers in a feasible and statistically powerful way.

Gene flow favours local adaptation under habitat choice in ciliate microcosms.

Local adaptation is assumed to occur under limited gene flow. However, habitat-matching theory predicts dispersal should favour rather than hinder local adaptation when individuals selectively disperse towards habitats maximizing their performance. We provide experimental evidence that local adaptation to the upper margin of a species' thermal niche is favoured by dispersal with habitat choice, but hindered under random dispersal. Our study challenges the idea that high gene flow precludes local adaptation, and provides unique experimental evidence of habitat choice as an overlooked mechanism responsible for adaptation under rapid environmental changes.

Cooperation-mediated plasticity in dispersal and colonization.

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density-dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density-dependent dispersal, whereas low-aggregation genotypes showed maximum dispersal rates at intermediate density, and medium-aggregation genotypes showed density-independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long-distance dispersal phenotypes, contrary to low-aggregation genotypes; medium-aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin-cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin-competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.

Flight Morphology, Compound Eye Structure and Dispersal in the Bog and the Cranberry Fritillary Butterflies: An Inter- and Intraspecific Comparison.

Understanding dispersal is of prime importance in conservation and population biology. Individual traits related to motion and navigation during dispersal may differ: (1) among species differing in habitat distribution, which in turn, may lead to interspecific differences in the potential for and costs of dispersal, (2) among populations of a species that experiences different levels of habitat fragmentation; (3) among individuals differing in their dispersal strategy and (4) between the sexes due to sexual differences in behaviour and dispersal tendencies. In butterflies, the visual system plays a central role in dispersal, but exactly how the visual system is related to dispersal has received far less attention than flight morphology. We studied two butterfly species to explore the relationships between flight and eye morphology, and dispersal. We predicted interspecific, intraspecific and intersexual differences for both flight and eye morphology relative to i) species-specific habitat distribution, ii) variation in dispersal strategy within each species and iii) behavioural differences between sexes. However, we did not investigate for potential population differences. We found: (1) sexual differences that presumably reflect different demands on both male and female visual and flight systems, (2) a higher wing loading (i.e. a proxy for flight performance), larger eyes and larger facet sizes in the frontal and lateral region of the eye (i.e. better navigation capacities) in the species inhabiting naturally fragmented habitat compared to the species inhabiting rather continuous habitat, and (3) larger facets in the frontal region in dispersers compared to residents within a species. Hence, dispersers may have similar locomotory capacity but potentially better navigation capacity. Dispersal ecology and evolution have attracted much attention, but there are still significant gaps in our understanding of the mechanisms of dispersal. Unfortunately, for many species we lack detailed information on the role of behavioural, morphological and physiological traits for dispersal. Our novel study supports the existence of inter- and intra-specific evolutionary responses in both motion and navigation capacities (i.e. flight and eye morphology) linked to dispersal.

BEMOVI, software for extracting behavior and morphology from videos, illustrated with analyses of microbes.

Microbes are critical components of ecosystems and provide vital services (e.g., photosynthesis, decomposition, nutrient recycling). From the diverse roles microbes play in natural ecosystems, high levels of functional diversity result. Quantifying this diversity is challenging, because it is weakly associated with morphological differentiation. In addition, the small size of microbes hinders morphological and behavioral measurements at the individual level, as well as interactions between individuals. Advances in microbial community genetics and genomics, flow cytometry and digital analysis of still images are promising approaches. They miss out, however, on a very important aspect of populations and communities: the behavior of individuals. Video analysis complements these methods by providing in addition to abundance and trait measurements, detailed behavioral information, capturing dynamic processes such as movement, and hence has the potential to describe the interactions between individuals. We introduce BEMOVI, a package using the R and ImageJ software, to extract abundance, morphology, and movement data for tens to thousands of individuals in a video. Through a set of functions BEMOVI identifies individuals present in a video, reconstructs their movement trajectories through space and time, and merges this information into a single database. BEMOVI is a modular set of functions, which can be customized to allow for peculiarities of the videos to be analyzed, in terms of organisms features (e.g., morphology or movement) and how they can be distinguished from the background. We illustrate the validity and accuracy of the method with an example on experimental multispecies communities of aquatic protists. We show high correspondence between manual and automatic counts and illustrate how simultaneous time series of abundance, morphology, and behavior are obtained from BEMOVI. We further demonstrate how the trait data can be used with machine learning to automatically classify individuals into species and that information on movement behavior improves the predictive ability.

Social information from immigrants: multiple immigrant-based sources of information for dispersal decisions in a ciliate.

1. Dispersal is increasingly recognized as being an informed process, based on information organisms obtain about the landscape. While local conditions are often found to drive dispersal decisions, local context is not always a reliable predictor of conditions in neighbouring patches, making the use of local information potentially useless or even maladaptive. In this case, using social information gathered by immigrants might allow adjusting dispersal decisions without paying the costs of prospecting. However, this hypothesis has been largely neglected despite its major importance for ecological and evolutionary processes. 2. We investigated three fundamental questions about immigrant-informed dispersal: Do immigrants convey information that influences dispersal, do organisms use multiple cues from immigrants, and is immigrant-informed dispersal genotype dependent? 33. Using Tetrahymena thermophila ciliates in microcosms, we manipulated the number of immigrants arriving, the density of congeners, the resource quality in neighbouring patches, matrix characteristics and the level of cooperation of individuals in the neighbouring populations. 4. We provide the first experimental evidence that immigrants convey a number of different cues about neighbouring patches and matrix (patch quality, matrix characteristics and cooperation in neighbouring populations) in this relatively simple organism. Furthermore, we demonstrate genotype-dependent immigrant-informed dispersal decisions about patch quality and matrix characteristics. 5. Multiple cues from immigrants and genotype-dependent use of cues have major implications for theoretical metapopulation dynamics and the potential for local adaptation.