Local adaptation in dispersal in multi‐resource landscapes

The distribution of resources in space has important consequences for the evolution of dispersal‐related traits. Dispersal moderates patterns of gene flow and, consequently, the potential for local adaptation to spatially differentiated resource types. We lack both models and experiments that evaluate how dispersal evolves in landscapes with multiple resources. Here, we investigate the evolution of dispersal in landscapes that contain two resource types that differ in their spatial autocorrelations. Individuals may possess ecological traits that give them a fitness advantage on one or the other resource. We find that resources differing in their spatial autocorrelation select for different optimal dispersal strategies and, further, that some multi‐resource landscapes can support the stable coexistence of distinct dispersal strategies. Whether divergence in dispersal strategies between resource specialists occurs depends on the underlying structure of the resources and the degree of linkage between dispersal strategies and ecological specialization. This work indicates that the spatial autocorrelation of resources is an important factor in determining when evolutionary branching is likely to occur, and sheds light on when secondary isolating mechanisms should arise between locally adapted specialists.     

The number of breeders explains genetic connectivity in an endangered bird

Connectivity is central to ecology and evolution as it focuses on the movement of individuals or genes across landscapes. Genetic connectivity approaches aim to understand gene flow but often estimate it indirectly based on metrics of genetic differentiation, which can also be affected by other evolutionary forces such as genetic drift. Gene flow and genetic drift are driven by separate ecological mechanisms with potentially differing effects on genetic differentiation and interpretations of genetic connectivity. The ecological mechanisms contributing to gene flow and genetic drift are primarily effective dispersal, or movement followed by successful reproduction, and the number of breeders in a local population, N_b, respectively. Yet, rarely are these ecological mechanisms and genetic connectivity measured simultaneously across landscapes. We examine the roles of effective dispersal and N_b on genetic connectivity across the entire range of the endangered snail kite (Rostrhamus sociabilis plumbeus), between 2006–2015. We find that both N_b and effective dispersal are important predictors of genetic connectivity across this landscape, but that N_b has a 3 × stronger effect on genetic connectivity. Furthermore, N_b is positively correlated with heterozygosity and allelic richness within patches, suggesting a potentially important role of genetic drift, in addition to gene flow, on genetic connectivity. These results emphasize that conservation efforts should focus on not only between‐patch processes of movement but also within‐patch processes regarding habitat quality and local population size for increasing genetic connectivity.     

Joint evolution of dispersal and connectivity

Functional connectivity, the realized flow of individuals between the suitable sites of a heterogeneous landscape, is a prime determinant of the maintenance and evolution of populations in fragmented habitats. While a large body of literature examines the evolution of dispersal propensity, it is less known how evolution shapes functional connectivity via traits that influence the distribution of the dispersers. Here, we use a simple model to demonstrate that, in a heterogeneous environment with clustered and solitary sites (i.e., with variable structural connectivity), the evolutionarily stable population contains strains that are strongly differentiated in their pattern of connectivity (local vs. global dispersal), but not necessarily in the fraction of dispersed individuals. Also during evolutionary branching, selection is disruptive predominantly on the pattern of connectivity rather than on dispersal propensity itself. Our model predicts diversification along a hitherto neglected axis of dispersal strategies and highlights the role of the solitary sites—the more isolated and therefore seemingly less important patches of habitat—in maintaining global dispersal that keeps all sites connected.     

Individual dispersal,landscape connectivity and ecological networks

Connectivity is classically considered an emergent property of landscapes encapsulating individuals' flows across space. However, its operational use requires a precise understanding of why and how organisms disperse. Such movements, and hence landscape connectivity, will obviously vary according to both organism properties and landscape features. We review whether landscape connectivity estimates could gain in both precision and generality by incorporating three fundamental outcomes of dispersal theory. Firstly, dispersal is a multi‐causal process; its restriction to an ‘escape reaction’ to environmental unsuitability is an oversimplification, as dispersing individuals can leave excellent quality habitat patches or stay in poor‐quality habitats according to the relative costs and benefits of dispersal and philopatry. Secondly, species, populations and individuals do not always react similarly to those cues that trigger dispersal, which sometimes results in contrasting dispersal strategies. Finally, dispersal is a major component of fitness and is thus under strong selective pressures, which could generate rapid adaptations of dispersal strategies. Such evolutionary responses will entail spatiotemporal variation in landscape connectivity. We thus strongly recommend the use of genetic tools to: (i) assess gene flow intensity and direction among populations in a given landscape; and (ii) accurately estimate landscape features impacting gene flow, and hence landscape connectivity. Such approaches will provide the basic data for planning corridors or stepping stones aiming at (re)connecting local populations of a given species in a given landscape. This strategy is clearly species‐ and landscape‐specific. But we suggest that the ecological network in a given landscape could be designed by stacking up such linkages designed for several species living in different ecosystems. This procedure relies on the use of umbrella species that are representative of other species living in the same ecosystem.     

Critical threshold effects of benthiscape structure on stream herbivore movement

In landscape ecology, substantial theoretical progress has been made in understanding how critical threshold levels of habitat loss may result in sudden changes in landscape connectivity to animal movement. Empirical evidence for such thresholds in real systems, however, remains scarce. Streambed landscapes provide a strong testing ground for studying critical thresholds because organisms are faced with substantial environmental heterogeneity while attempting to overcome the physical force of water. In this study, I report on the results from a series of experiments investigating the influence of habitat abundance and current velocity on the movement dynamics of two stream herbivores (caddisfly larva Agapetus boulderensis and snail Physa sp.) that differ substantially in how they perceive landscape structure. Specifically, I ask whether critical thresholds to herbivore movement exist in streambed landscapes. By exploiting the pattern recognition capabilities of artificial neural networks, I found that the rate, sinuosity and directionality of movement by Agapetus and Physa varied nonlinearly according to the abundance of habitat patches, current velocity and habitat-current interaction. Both the study organisms exhibited threshold responses to habitat abundance, yet the location and slope of these thresholds differed between species and with respect to different current velocities. These results suggest that a critical threshold in functional connectivity (i.e. the connection of habitat patches by dispersal) is not an inherent property of the landscape, but in fact emerges from the interplay of species' interactions with landscape structure. Moreover, current velocity interacted with habitat abundance to elicit strong upstream-oriented movement for both the species. This suggests that dispersing individuals may be polarized in the upstream direction and therefore functional connectivity is not equal in all directions. Such results highlight the need for future research addressing the sources of variability of critical threshold effects in ecological phenomena.     

Metapopulation-level adaptation of insect host plant preference and extinction-colonization dynamics in heterogeneous landscapes

Species living in highly fragmented landscapes typically occur as metapopulations with frequent turnover of local populations. The turnover rate depends on population sizes and connectivities, but it may also depend on the phenotypic and genotypic composition of populations. The Glanville fritillary butterfly (Melitaea cinxia) in Finland uses two host plant species, which show variation in their relative abundances at two spatial scales: locally among individual habitat patches and regionally among networks of patches. Female butterflies in turn exhibit spatial variation in genetically determined host plant preference within and among patch networks. Emigration, immigration and establishment of new populations have all been shown to be strongly influenced by the match between the host plant composition of otherwise suitable habitat patches and the host plant preference of migrating butterflies. The evolutionary consequences of such biased migration and colonization with respect to butterfly phenotypes might differ depending on spatial configuration and plant species composition of the patches in heterogeneous patch networks. Using a spatially realistic individual-based model we show that the model-predicted evolution of host plant preference due to biased migration explains a significant amount of the observed variation in host plant use among metapopulations living in dissimilar networks. This example illustrates how the ecological extinction-colonization dynamics may be linked with the evolutionary dynamics of life history traits in metapopulations.     

Habitat choice stabilizes metapopulation dynamics by enabling ecological specialization

Dispersal is a key trait responsible for the spread of individuals and genes among local populations, thereby generating eco‐evolutionary interactions. Especially in heterogeneous metapopulations, a tight coupling between dispersal, population dynamics and the evolution of local adaptation is expected. In this respect, dispersal should counteract ecological specialization by redistributing locally selected phenotypes (i.e. migration load). Habitat choice following an informed dispersal decision, however, can facilitate the evolution of ecological specialization. How such informed decisions influence metapopulation size and variability is yet to be determined. By means of individual‐based modelling, we demonstrate that informed decisions about both departure and settlement decouple the evolution of dispersal and that of generalism, selecting for highly dispersive specialists. Choice at settlement is based on information from the entire dispersal range, and therefore decouples dispersal from ecological specialization more effectively than choice at departure, which is only based on local information. Additionally, habitat choice at departure and settlement reduces local and metapopulation variability because of the maintenance of ecological specialization at all levels of dispersal propensity. Our study illustrates the important role of habitat choice for dynamics of spatially structured populations and thus emphasizes the importance of considering that dispersal is often informed.     

Between migration load and evolutionary rescue: dispersal,adaptation and the response of spatially structured populations to environmental change

The evolutionary potential of populations is mainly determined by population size and available genetic variance. However, the adaptability of spatially structured populations may also be affected by dispersal: positively by spreading beneficial mutations across sub-populations, but negatively by moving locally adapted alleles between demes. We develop an individual-based, two-patch, allelic model to investigate the balance between these opposing effects on a population''s evolutionary response to rapid climate change. Individual fitness is controlled by two polygenic traits coding for local adaptation either to the environment or to climate. Under conditions of selection that favour the evolution of a generalist phenotype (i.e. weak divergent selection between patches) dispersal has an overall positive effect on the persistence of the population. However, when selection favours locally adapted specialists, the beneficial effects of dispersal outweigh the associated increase in maladaptation for a narrow range of parameter space only (intermediate selection strength and low linkage among loci), where the spread of beneficial climate alleles is not strongly hampered by selection against non-specialists. Given that local selection across heterogeneous and fragmented landscapes is common, the complex effect of dispersal that we describe will play an important role in determining the evolutionary dynamics of many species under rapidly changing climate.     

Population structure inhibits evolutionary diversification under competition for resources

A model is presented that explores how population structure affects the evolutionary outcome of ecological competition for resources. The model assumes that competition for resources occurs within groups of a finite number of individuals (interaction groups), and that limited dispersal of individuals between groups (according to Wright's island model of population structure) results in genetic structuring of the population. It is found that both finite-sized interaction groups and limited dispersal can have substantial effects on the evolution of resource exploitation strategies as compared to models with a single, infinitely large, well-mixed interaction group. Both effects, in general, tend to select for less aggressive competitive strategies. Moreover, both effects also tend to reduce the likelihood of the evolutionary diversification of resource exploitation strategies that often occurs in models of resource competition with infinite populations. The results are discussed in the context of theories of the evolutionary diversification of resource exploitation strategies and speciation.     

Adaptive Patch Searching Strategies in Fragmented Landscapes

The search strategies dispersers employ to search for new habitat patches affect individuals’ search success and subsequently landscape connectivity and metapopulation viability. Some evidence indicates that individuals within the same species may display a variety of behavioural patch searching strategies rather than one species-specific strategy. This may result from landscape heterogeneity. We modelled the evolution of individual patch searching strategies in different landscapes. Specifically, we analysed whether evolution can favour different, co-existing, behavioural search strategies within one population and to what extent this coexistence of multiple strategies was dependent on landscape configuration. Using an individual-based simulation model, we studied the evolution of patch searching strategies in three different landscape configurations: uniform, random and clumped. We found that landscape configuration strongly influenced the evolved search strategy. In uniform landscapes, one fixed search strategy evolved for the entire spatially structured population, while in random and clumped landscapes, a set of different search strategies emerged. The coexistence of several search strategies also strongly depended on the dispersal mortality. We show that our result can affect landscape connectivity and metapopulation dynamics. Co-ordinating editor: N. Yamamura     

Evolutionary responses of dispersal distance to landscape structure and habitat loss

It is generally well understood that some ecological factors select for increased and others for decreased dispersal. However, it has remained difficult to assess how the evolutionary dynamics are influenced by the spatio-temporal structure of the environment. We address this question with an individual-based model that enables habitat structure to be controlled through variables such as patch size, patch turnover rate, and patch quality. Increasing patch size at the expense of patch density can select for more or less dispersal, depending on the initial configuration. In landscapes consisting of high-quality and long-lived habitat patches, patch degradation selects for increased dispersal, yet patch loss may select for reduced dispersal. These trends do not depend on the component of life-history that is affected by habitat quality or the component of life-history through which density-dependence operates. Our results are based on a mathematical method that enables derivation of both the evolutionary stable strategy and the stationary genotype distribution that evolves in a polymorphic population. The two approaches generally lead to similar predictions. However, the evolutionary stable strategy assumes that the ecological and evolutionary time scales can be separated, and we find that violation of this assumption can critically alter the evolutionary outcome.     

Proximity of restored hedgerows interacts with local floral diversity and species' traits to shape long‐term pollinator metacommunity dynamics

Disconnected habitat fragments are poor at supporting population and community persistence; restoration ecologists, therefore, advocate for the establishment of habitat networks across landscapes. Few empirical studies, however, have considered how networks of restored habitat patches affect metacommunity dynamics. Here, using a 10‐year study on restored hedgerows and unrestored field margins within an intensive agricultural landscape, we integrate occupancy modelling with network theory to examine the interaction between local and landscape characteristics, habitat selection and dispersal in shaping pollinator metacommunity dynamics. We show that surrounding hedgerows and remnant habitat patches interact with the local floral diversity, bee diet breadth and bee body size to influence site occupancy, via colonisation and persistence dynamics. Florally diverse sites and generalist, small‐bodied species are most important for maintaining metacommunity connectivity. By providing the first in‐depth assessment of how a network of restored habitat influences long‐term population dynamics, we confirm the conservation benefit of hedgerows for pollinator populations and demonstrate the importance of restoring and maintaining habitat networks within an inhospitable matrix.     

Gene networks and metacommunities: dispersal differences can override adaptive advantage

Dispersal is an important mechanism contributing to both ecological and evolutionary dynamics. In metapopulation and metacommunity ecology, dispersal enables new patches to be colonized; in evolution, dispersal counter-acts local selection, leading to regional homogenization. Here, I consider a three-patch metacommunity in which two species, each with a limiting quantitative trait underlain by gene networks of 16 to 256 genes, compete with one another and disperse among patches. Incorporating dispersal among heterogeneous patches introduces a tradeoff not observed in single-patch simulations: if the difference between gene network size of the two species is greater than the difference in dispersal ability (e.g., if the ratio of network sizes is larger than the ratio of dispersal abilities), then genetic architecture drives community outcome. However, if the difference in dispersal abilities is greater than gene network differences, then any adaptive advantages afforded by genetic architecture are over-ridden by dispersal. Thus, in addition to the selective pressures imposed by competition that shape the genetic architecture of quantitative traits, dispersal among patches creates an escape that may further alter the effects of different genetic architectures. These results provide a theoretical expectation for what we may observe as the field of ecological genomics develops.     

Dispersal evolution in temporally variable environments: implications for plant range dynamics

Dispersal—the movement of an individual from the site of birth to a different site for reproduction—is an ecological and evolutionary driver of species ranges that shapes patterns of colonization, connectivity, gene flow, and adaptation. In plants, the traits that influence dispersal often vary within and among species, are heritable, and evolve in response to the fitness consequences of moving through heterogeneous landscapes. Spatial and temporal variation in the quality and quantity of habitat are important sources of selection on dispersal strategies across species ranges. While recent reviews have evaluated the interactions between spatial variation in habitat and dispersal dynamics, the extent to which geographic variation in temporal variability can also shape range-wide patterns in dispersal traits has not been synthesized. In this paper, we summarize key predictions from metapopulation models that evaluate how dispersal evolves in response to spatial and temporal habitat variability. Next, we compile empirical data that quantify temporal variability in plant demography and patterns of dispersal trait variation across species ranges to evaluate the hypothesis that higher temporal variability favors increased dispersal at plant range limits. We found some suggestive evidence supporting this hypothesis while more generally identifying a major gap in empirical work evaluating plant metapopulation dynamics across species ranges and geographic variation in dispersal traits. To address this gap, we propose several future research directions that would advance our understanding of the interplay between spatiotemporal variability and dispersal trait variation in shaping the dynamics of current and future species ranges.     

From dispersal constraints to landscape connectivity: lessons from species distribution modeling

Connectivity plays a crucial role in determining the spread, viability, and persistence of populations across space. Dispersal across landscapes, or the movement of individuals or genes among resource patches, is critical for functional connectivity. Yet current connectivity modelling typically uses information on species location or habitat preference rather than movement, which unfortunately may not capture key dispersal limitations. We argue that recent developments in species distribution modelling provide insightful lessons for addressing this gap and advancing our understanding of connectivity. We suggest shifting the focus of connectivity modelling from locating where animals potentially disperse to a process‐based approach directed towards understanding and mapping factors that limit successful dispersal. To do so, we propose defining species dispersal requirements through identifying spatial, environmental and intrinsic constraints to successful dispersal, analogous to identifying environmental dimensions that define niches. We discuss the benefits of this constraint‐based framework for understanding the distribution of species, predicting species responses to climate change, and connectivity conservation practice. We illustrate how the framework can aid in identifying potential detrimental effects of human activities on connectivity and species persistence, and can spur the implementation of innovative conservation strategies. The proposed framework clarifies the validity and contextual utility of objectives and measures in existing connectivity models, and identifies gaps that may impede our understanding of connectivity and its integration into successful conservation strategies. We expect that this framework will facilitate a mechanistic approach to understanding and conserving connectivity, which will aid in effectively predicting and mitigating effects of ongoing environmental change.     

The evolution of patch selection in stochastic environments

A null model for habitat patch selection in spatially heterogeneous environments is the ideal free distribution (IFD), which assumes individuals have complete knowledge about the environment and can freely disperse. Under equilibrium conditions, the IFD predicts that local population growth rates are zero in all occupied patches, sink patches are unoccupied, and the fraction of the population selecting a patch is proportional to the patch's carrying capacity. Individuals, however, often experience stochastic fluctuations in environmental conditions and cannot respond to these fluctuations instantaneously. An evolutionary stability analysis for fixed patch-selection strategies reveals that environmental uncertainty disrupts the classical IFD predictions: individuals playing the evolutionarily stable strategy may occupy sink patches, local growth rates are negative and typically unequal in all patches, and individuals prefer higher-quality patches less than predicted by their carrying capacities. Spatial correlations in environmental fluctuations can enhance or marginalize these trends. The analysis predicts that continually increasing environmental variation first selects for range expansion, then selects for persisting coupled sink populations, and ultimately leads to regional extinction. In contrast, continually increasing habitat degradation first selects for range contraction and may select for persisting coupled sink populations before regional extinction. These results highlight the combined roles of spatial and temporal heterogeneity on the evolution of habitat selection.     

Evolution of positive and negative density-dependent dispersal

Understanding the evolution of density-dependent dispersal strategies has been a major challenge for evolutionary ecologists. Some existing models suggest that selection should favour positive and others negative density-dependence in dispersal. Here, we develop a general model that shows how and why selection may shift from positive to negative density-dependence in response to key ecological factors, in particular the temporal stability of the environment. We find that in temporally stable environments, particularly with low dispersal costs and large group sizes, habitat heterogeneity selects for negative density-dependent dispersal, whereas in temporally variable environments, particularly with high dispersal costs and small group sizes, habitat heterogeneity selects for positive density-dependent dispersal. This shift reflects the changing balance between the greater competition for breeding opportunities in more productive patches, versus the greater long-term value of offspring that establish themselves there, the latter being very sensitive to the temporal stability of the environment. In general, dispersal of individuals out of low-density patches is much more sensitive to habitat heterogeneity than is dispersal out of high-density patches.     

Functional connectivity in replicated urban landscapes in the land snail (Cornu aspersum)

Urban areas are highly fragmented and thereby exert strong constraints on individual dispersal. Despite this, some species manage to persist in urban areas, such as the garden snail, Cornu aspersum, which is common in cityscapes despite its low mobility. Using landscape genetic approaches, we combined study area replication and multiscale analysis to determine how landscape composition, configuration and connectivity influence snail dispersal across urban areas. At the overall landscape scale, areas with a high percentage of roads decreased genetic differentiation between populations. At the population scale, genetic differentiation was positively linked with building surface, the proportion of borders where wooded patches and roads appeared side by side and the proportion of borders combining wooded patches and other impervious areas. Analyses based on pairwise genetic distances validated the isolation‐by‐distance and isolation‐by‐resistance models for this land snail, with an equal fit to least‐cost paths and circuit‐theory‐based models. Each of the 12 landscapes analysed separately yielded specific relations to environmental features, whereas analyses integrating all replicates highlighted general common effects. Our results suggest that urban transport infrastructures facilitate passive snail dispersal. At a local scale, corresponding to active dispersal, unfavourable habitats (wooded and impervious areas) isolate populations. This work upholds the use of replicated landscapes to increase the generalizability of landscape genetics results and shows how multiscale analyses provide insight into scale‐dependent processes.     

Divergent evolution of dispersal in a heterogeneous landscape

The evolution of dispersal is investigated in a landscape of many patches with fluctuating carrying capacities and spatial heterogeneity in temporal fluctuations. Although asynchronous temporal fluctuations select for dispersal, spatial heterogeneity in the distribution of fluctuating environmental variables selects against it. We find evolutionary branching in dispersal rate leading to the evolutionarily stable coexistence of a high- and a low-dispersal phenotype. We study how the opposing forces of selection for and against dispersal change with the relative size and the environmental qualities of the source and sink habitats. Our results suggest that the evolution of dispersal dimorphism could be a first step towards speciation and local adaptation.     

Classical metapopulation dynamics and eco‐evolutionary feedbacks in dendritic networks

Eco‐evolutionary dynamics are now recognized to be highly relevant for population and community dynamics. However, the impact of evolutionary dynamics on spatial patterns, such as the occurrence of classical metapopulation dynamics, is less well appreciated. Here, we analyse the evolutionary consequences of spatial network connectivity and topology for dispersal strategies and quantify the eco‐evolutionary feedback in terms of altered classical metapopulation dynamics. We find that network properties, such as topology and connectivity, lead to predictable spatio‐temporal correlations in fitness expectations. These spatio‐temporally stable fitness patterns heavily impact evolutionarily stable dispersal strategies and lead to eco‐evolutionary feedbacks on landscape level metrics, such as the number of occupied patches, the number of extinctions and recolonizations as well as metapopulation extinction risk and genetic structure. Our model predicts that classical metapopulation dynamics are more likely to occur in dendritic networks, and especially in riverine systems, compared to other types of landscape configurations. As it remains debated whether classical metapopulation dynamics are likely to occur in nature at all, our work provides an important conceptual advance for understanding the occurrence of classical metapopulation dynamics which has implications for conservation and management of spatially structured populations.