Maxime Dahirel

Movement propensity and ability correlate with ecological specialization in European land snails: comparative analysis of a dispersal syndrome

Intra- and interspecific differences in movement behaviour play an important role in the ecology and evolution of animals, particularly in fragmented landscapes. As a consequence of rarer and generally more fragmented habitat, and because dispersal tends to disrupt benefits brought by local adaptation, theory predicts that mobility and dispersal should be counter-selected in specialists. Using experimental data and phylogenetic comparative tools, we analysed movement propensity and capacity, as well as dispersal-related phenotypic traits, in controlled conditions in 20 species of European land snails from the Helicoidea superfamily. Costs of movement in terrestrial gastropods are among the highest in animals, which make them a potentially powerful model to test these predictions. Habitat specialists were indeed less likely to cross a boundary between a familiar and an unfamiliar substrate than generalists. They also had smaller feet, after accounting for size. Furthermore, exploring specialists were slower than generalists and had more tortuous trajectories, leading them to stay closer to the familiar patch. Movement traits were generally evolutionary labile, but some were constrained by body size, a phylogenetically conserved trait. High specialization and low-dispersal ability are two traits often considered to increase species vulnerability to fragmentation, climate changes and extinction. This study confirms they should not be considered separately, due to their integration in a dispersal syndrome. Therefore, specialist species face double penalty under habitat loss and other environmental changes, making them more vulnerable to extinction and contributing to the biotic homogenization of communities.

Body-size shifts in aquatic and terrestrial urban communities

Body size is intrinsically linked to metabolic rate and life-history traits, and is a crucial determinant of food webs and community dynamics1,2. The increased temperatures associated with the urban-heat-island effect result in increased metabolic costs and are expected to drive shifts to smaller body sizes3. Urban environments are, however, also characterized by substantial habitat fragmentation4, which favours mobile species. Here, using a replicated, spatially nested sampling design across ten animal taxonomic groups, we show that urban communities generally consist of smaller species. In addition, although we show urban warming for three habitat types and associated reduced community-weighted mean body sizes for four taxa, three taxa display a shift to larger species along the urbanization gradients. Our results show that the general trend towards smaller-sized species is overruled by filtering for larger species when there is positive covariation between size and dispersal, a process that can mitigate the low connectivity of ecological resources in urban settings5. We thus demonstrate that the urban-heat-island effect and urban habitat fragmentation are associated with contrasting community-level shifts in body size that critically depend on the association between body size and dispersal. Because body size determines the structure and dynamics of ecological networks1, such shifts may affect urban ecosystem function.The urban-heat-island effect drives community-level shifts towards smaller body sizes; however, habitat fragmentation caused by urbanization favours larger body sizes in species with positive size–dispersal links.

Kin competition accelerates experimental range expansion in an arthropod herbivore

With ongoing global change, life is continuously forced to move to novel areas, which leads to dynamically changing species ranges. As dispersal is central to range dynamics, factors promoting fast and distant dispersal are key to understanding and predicting species ranges. During range expansions, genetic variation is depleted at the expanding front. Such conditions should reduce evolutionary potential, while increasing kin competition. Organisms able to recognise relatives may be able to assess increased levels of relatedness at expanding range margins and to increase their dispersal in a plastic manner. Using individual-based simulations and experimental range expansions of a spider mite, we demonstrate that plastic responses to kin structure can be at least as important as evolution in driving range expansion speed. Because recognition of kin or kind is increasingly documented across the tree of life, we anticipate it to be a highly important but neglected driver of range expansions.

Density-dependence across dispersal stages in a hermaphrodite land snail: insights from discrete choice models

Dispersal movements, i.e. movements leading to gene flow, are key behaviours with important, but only partially understood, consequences for the dynamics and evolution of populations. In particular, density-dependent dispersal has been widely described, yet how it is determined by the interaction with individual traits, and whether density effects differ between the three steps of dispersal (departure, transience, and settlement), remains largely unknown. Using a semi-natural landscape, we studied dispersal choices of Cornu aspersum land snails, a species in which negative effects of crowding are well documented, and analysed them using dispersal discrete choice models, a new method allowing the analysis of dispersal decisions by explicitly considering the characteristics of all available alternatives and their interaction with individual traits. Subadults were more dispersive than adults, confirming existing results. In addition, departure and settlement were both density dependent: snails avoided crowded patches at both ends of the dispersal process, and subadults were more reluctant to settle into crowded patches than adults. Moreover, we found support for carry-over effects of release density on subsequent settlement decisions: snails from crowded contexts were more sensitive to density in their subsequent immigration choices. The fact that settlement decisions were informed indicates that costs of prospecting are not as important as previously thought in snails, and/or that snails use alternative ways to collect information, such as indirect social information (e.g. trail following). The observed density-dependent dispersal dynamics may play an important role in the ability of C. aspersum to successfully colonise frequently human-disturbed habitats around the world.

Dispersal: a central trait in life history

The study of trade-offs among major life history components (age at maturity, lifespan and reproduction) allowed the development of a quantitative framework to understand how environmental variation shapes patterns of biodiversity among and within species. Because every environment is inherently spatially structured, and in most cases temporally variable, individuals need to move within and among habitats to maximize fitness. Dispersal is often assumed to be tightly integrated into life histories through genetic correlations with other vital traits. This assumption is particularly strong within the context of a fast-slow continuum of life-history variation. Such a framework is to date used to explain many aspects of population and community dynamics. Evidence for a consistent and context-independent integration of dispersal in life histories is, however, weak. We therefore advocate the explicit integration of dispersal into life history theory as a principal axis of variation influencing fitness, that is free to evolve, independently of other life history traits. We synthesize theoretical and empirical evidence on the central role of dispersal and its evolutionary dynamics on the spatial distribution of ecological strategies and its impact on population spread, invasions and coexistence. By applying an optimality framework we show that the inclusion of dispersal as an independent dimension of life histories might substantially change our view on evolutionary trajectories in spatially structured environments. Because changes in the spatial configuration of habitats affect the costs of movement and dispersal, adaptations to reduce these costs will increase phenotypic divergence among and within populations. We outline how this phenotypic heterogeneity is anticipated to further impact population and community dynamics.

Urbanization-driven changes in web-building are decoupled from body size in an orb-web spider

In animals, behavioural responses may play an important role in determining population persistence in the face of environmental changes. Body size is a key trait central to many life history traits and behaviours. While behaviours are typically assumed to be highly plastic, size correlations may impose constraints on their adaptive value when size itself is subject to environmental changes. Urbanization is an important human-induced environmental change that imposes multiple selection pressures on both body size and (size-constrained) behaviour. How these combine to shape behavioural responses of urban-dwelling species is unclear. Using web-building behaviour, an easily quantifiable behaviour linked to body size, and the garden spider Araneus diadematus as a model, we disentangle direct behavioural responses to urbanization and body size constraints across a network of 63 selected populations differing in urbanization intensity at two spatial scales. Spiders were smaller in highly urbanized sites (local scale only), in line with reduced prey availability and the urban heat island effect. The use of piecewise structural equation modelling reveals that despite existing size constraints on web-building behaviour, these size shifts overall have a minor effect on web-building response to urbanization. Spiders altered their web-building behaviours in response to urbanization in ways that are expected to compensate, at least in part, for reduced prey availability. Different components of web-building reacted to urbanization at different scales, which may indicate different balances between the effects of genetic adaptation and plasticity. Although fecundity decreased with local-scale urbanization, Araneus diadematus abundance stayed remarkably stable across urbanization gradients, independently of scale and intensity, meaning this strategy appears overall successful at the population level. Our results demonstrate that typically responses in size-dependent behaviours may be decoupled from size-correlations, thereby allowing fitness maximisation in novel environments.In animals, behavioural responses may play an important role in determining population persistence in the face of environmental changes. Body size is a key trait central to many life history traits and behaviours. While behaviours are typically assumed to be highly plastic, size correlations may impose constraints on their adaptive value when size itself is subject to environmental changes. Urbanization is an important human-induced rapid environmental change that imposes multiple selection pressures on both body size and (size-constrained) behaviour. How these combine to shape behavioural responses of urban-dwelling species is unclear. Using web-building, an easily quantifiable behaviour linked to body size, and the garden spider Araneus diadematus as a model, we disentangle direct behavioural responses to urbanization and body size constraints across a network of 63 selected populations differing in urbanization intensity at two spatial scales. Spiders were smaller in highly urbanized sites (local scale only), in line with expectations based on reduced prey biomass availability and the Urban Heat Island effect. The use of multivariate mixed modelling reveals that although web traits and body size are correlated within populations, behavioural responses to urbanization do not appear to be constrained by size: there is no evidence of size-web correlations among populations or among landscapes. Spiders thus altered different components of their web-building behaviours independently in response to urbanization: mesh width and web surface decreased independently with urbanization at the local scale, while web surface also increased with urbanization at the landscape scale. These responses are expected to compensate, at least in part, for reduced prey biomass availability. Our results demonstrate that responses in typically size-dependent behaviours may be decoupled from size changes, thereby allowing fitness maximisation in novel environments. The spatial scale of the behavioural responses to urbanization suggest contributions of both genetic adaptation and plasticity. Although fecundity decreased with local-scale urbanization, Araneus diadematus abundances were remarkably similar across urbanization gradients; behavioural responses thus appear overall successful at the population level.

Dispersers are more likely to follow mucus trails in the land snail Cornu aspersum

Dispersal, i.e. movement leading to gene flow, is a fundamental although costly life history trait. The use of indirect social information may help mitigate these costs, yet in many cases little is known about the proximate sources of such information, and how dispersers and residents may differ in their information use. Land gastropods, which have a high cost of movement and obligatorily leave information potentially exploitable by conspecifics during movement (through mucus trails), are a good model to investigate links between dispersal costs and information use. We used Y-mazes to see whether dispersers and residents differed in their trail-following propensity, in the snail Cornu aspersum. Dispersers followed mucus trails more frequently than expected by chance, contrary to non-dispersers. Ignoring dispersal status during tests would lead to falsely conclude to no trail-following for the majority of ecologically realistic scenarios. Trail following by dispersers may reduce dispersal costs by reducing energy expenditure and helping snails find existing patches. Finally, we point that ignoring the potential for collective dispersal provided by trail-following abilities may lead to wrong inferences on the demographic and genetic consequences of dispersal.

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.In a coordinated distributed dispersal experiment involving seven laboratories, the authors show that both top-down predation risk and bottom-up resource limitation increase emigration rates across 21 species ranging from protozoa to vertebrates.

Urbanization-driven changes in web building and body size in an orb web spider

In animals, behavioural responses may play an important role in determining population persistence in the face of environmental changes. Body size is a key trait central to many life-history traits and behaviours. Correlations with body size may constrain behavioural variation in response to environmental changes, especially when size itself is influenced by environmental conditions. Urbanization is an important human-induced rapid environmental change that imposes multiple selection pressures on both body size and (size-constrained) behaviour. How these combine to shape behavioural responses of urban-dwelling species is unclear. Using web building, an easily quantifiable behaviour linked to body size and the garden spider Araneus diadematus as a model, we evaluated direct behavioural responses to urbanization and body size constraints across a network of 63 selected populations differing in urbanization intensity. We additionally studied urbanization at two spatial scales to account for some environmental pressures varying across scales and to obtain first qualitative insights about the role of plasticity and genetic selection. Spiders were smaller in highly urbanized sites (local scale only), in line with expectations based on reduced prey biomass availability and the Urban Heat Island effect. Web surface and mesh width decreased with urbanization at the local scale, while web surface also increased with urbanization at the landscape scale. The latter two responses are expected to compensate, at least in part, for reduced prey biomass availability in cities. The use of multivariate mixed modelling reveals that although web traits and body size are correlated within populations, behavioural responses to urbanization do not appear to be constrained by size: there is no evidence of size-web correlations among populations or among landscapes, and web traits appear independent from each other. Our results demonstrate that responses in size-dependent behaviours may be decoupled from size changes, thereby allowing fitness maximization in novel environments. The spatial scale at which traits respond suggests contributions of both genetic adaptation (for web investment) and plasticity (for mesh width). Although fecundity decreased with local-scale urbanization, A. diadematus abundances were similar across urbanization gradients; behavioural responses thus appear overall successful at the population level.

Kin competition overrules spatial selection as a driver of range expansions

With ongoing global change, life is continuously forced to move to novel areas, which leads to dynamically changing species ranges. As dispersal is central to range dynamics, factors promoting fast and distant dispersal are key to understanding and predicting species ranges. During range expansions, genetic variation is depleted at the expanding front. Such conditions should reduce evolutionary potential, while increasing kin competition. Organisms able to recognise relatives may be able to assess increased levels of relatedness at expanding range margins and to increase their dispersal in a plastic manner. Using individual-based simulations and experimental range expansions of a spider mite, we demonstrate that plastic responses to kin structure can be at least as important as evolution in driving range expansion speed. Because recognition of kin or kind is increasingly documented across the tree of life, we anticipate it to be a highly important but neglected driver of range expansions.With ongoing global change, life is continuously forced to move to novel areas, imposing rapid changes in biotic communities and ecosystem functioning. As dispersal is central to range dynamics, factors promoting fast and distant dispersal are key to understanding and predicting range expansions. As the range expands, genetic variation is strongly depleted and genetic homogenisation increases. Such conditions should reduce evolutionary potential, but also impose severe kin competition. Although kin competition drives dispersal, we lack insights into its contribution to range expansions, relative to other causal processes. To separate evolutionary dynamics from kin competition, we combined simulation modelling and experimental range expansion using the spider mite Tetranychus urticae. Both modelling and experimental evolution demonstrated that plastic responses to kin structure increased range expansion speed by about 20%, while the effects of evolution and spatial sorting were marginal. This insight resolves an important paradox between the loss of genetic variation and earlier observed evolutionary dynamics facilitating range expansions. Kin competition may thus provide a social rescue mechanism in populations that are forced to keep up with fast climate change.With ongoing global change, life is continuously forced to move to novel areas, imposing rapid changes in biotic communities and ecosystem functioning. As dispersal is central to range dynamics, factors promoting fast and distant dispersal are key to understanding and predicting range expansions. As the range expands, genetic variation is strongly depleted and genetic homogenisation increases. Such conditions should reduce evolutionary potential, but also impose severe kin competition. Although kin competition drives dispersal, we lack insights into its contribution to range expansions, relative to other causal processes. To separate evolutionary dynamics from kin competition, we combined simulation modelling and experimental range expansion using the spider mite Tetranychus urticae. Both modelling and experimental evolution demonstrated that plastic responses to kin structure increased range expansion speed by about 20%, while the effects of evolution and spatial sorting were marginal. This insight resolves an important paradox between the loss of genetic variation and earlier observed evolutionary dynamics facilitating range expansions. Kin competition may thus provide a social rescue mechanism in populations that are forced to keep up with fast climate change.