Evolution of dispersal polymorphism and local adaptation of dispersal distance in spatially structured landscapes

Many organisms show polymorphism in dispersal distance strategies. This variation is particularly ecological relevant if it encompasses a functional separation of short‐ (SDD) and long‐distance dispersal (LDD). It remains, however, an open question whether both parts of the dispersal kernel are similarly affected by landscape related selection pressures. We implemented an individual‐based model to analyze the evolution of dispersal traits in fractal landscapes that vary in the proportion of habitat and its spatial configuration. Individuals are parthenogenetic with dispersal distance determined by two alleles on each individual's genome: one allele coding for the probability of global dispersal and one allele coding for the variance σ of a Gaussian local dispersal with mean value zero. Simulations show that mean distances of local dispersal and the probability of global dispersal, increase with increasing habitat availability, but that changes in the habitat's spatial autocorrelation impose opposing selective pressure: local dispersal distances decrease and global dispersal probabilities increase with decreasing spatial autocorrelation of the available habitat. Local adaptation of local dispersal distance emerges in landscapes with less than 70% of clumped habitat. These results demonstrate that long and short distance dispersal evolve separately according to different properties of the landscape. The landscape structure may consequently largely affect the evolution of dispersal distance strategies and the level of dispersal polymorphism.     

Estimating dispersal distributions at multiple scales: within‐colony and among‐colony dispersal rates,distances and directions in European Shags Phalacrocorax aristotelis

Knowledge of the rate, distance and direction of dispersal within and among breeding areas is required to understand and predict demographic and genetic connectivity and resulting population and evolutionary dynamics. However dispersal rates, and the full distributions of dispersal distances and directions, are rarely comprehensively estimated across all spatial scales relevant to wild populations. We used re‐sightings of European Shags Phalacrocorax aristotelis colour‐ringed as chicks on the Isle of May (IoM), UK, to quantify rates, distances and directions of dispersal from natal to subsequent breeding sites both within IoM (within‐colony dispersal) and across 27 other breeding colonies covering 1045 km of coastline (among‐colony dispersal). Additionally, we used non‐breeding season surveys covering 895 km of coastline to estimate breeding season detection probability and hence potential bias in estimated dispersal parameters. Within IoM, 99.6% of individuals dispersed between their natal and observed breeding nest‐site. The distribution of within‐colony dispersal distances was right‐skewed; mean distance was shorter than expected given random settlement within IoM, yet some individuals dispersed long distances within the colony. The distribution of within‐colony dispersal directions was non‐uniform but did not differ from expectation given the spatial arrangement of nest‐sites. However, 10% of all 460 colour‐ringed adults that were located breeding had dispersed to a different colony. The maximum observed dispersal distance (170 km) was much smaller than the maximum distance surveyed (690 km). The distribution of among‐colony dispersal distances was again right‐skewed. Among‐colony dispersal was directional, and differed from random expectation and from the distribution of within‐colony dispersal directions. Non‐breeding season surveys suggested that the probability of detecting a colour‐ringed adult at its breeding location was high in the northeastern UK (98%). Estimated dispersal rates and distributions were therefore robust to incomplete detection. Overall, these data demonstrate skewed and directionally divergent dispersal distributions across small (within‐colony) and large (among‐colony) scales, indicating that dispersal could create genetic and demographic connectivity within the study area.     

Human-mediated dispersal of seeds over long distances

Human activities have fundamental impacts on the distribution of species through altered land use, but also directly by dispersal of propagules. Rare long-distance dispersal events have a disproportionate importance for the spread of species including invasions. While it is widely accepted that humans may act as vectors of long-distance dispersal, there are few studies that quantify this process. We studied in detail a mechanism of human-mediated dispersal (HMD). For two plant species we measured, over a wide range of distances, how many seeds are carried by humans on shoes. While over half of the seeds fell off within 5m, seeds were regularly still attached to shoes after 5 km. Semi-mechanistic models were fitted, and these suggested that long-distance dispersal on shoes is facilitated by decreasing seed detachment probability with distance. Mechanistic modelling showed that the primary vector, wind, was less important as an agent of long-distance dispersal, dispersing seeds less than 250 m. Full dispersal kernels were derived by combining the models for primary dispersal by wind and secondary dispersal by humans. These suggest that walking humans can disperse seeds to very long distances, up to at least 10 km, and provide some of the first quantified dispersal kernels for HMD.     

Biodiversity and ecosystem functioning: It is time for dispersal experiments

The experimental study of the relationship between biodiversity and ecosystem function has mainly addressed the effect of species and number of functional groups. In theory, this approach has mainly focused on how extinction affects function, whereas dispersal limitation of ecosystem function has been rarely discussed. A handful of seed introduction experiments, as well as numerous observations of the effects of long‐distance dispersal of alien species, indicate that ecosystem function may be strongly determined by dispersal limitation at the local, regional and/or global scales. We suggest that it is time to replace biodiversity manipulation experiments, based on random draw of species, with those addressing realistic scenarios of either extinction or dispersal. Experiments disentangling the dispersal limitation of ecosystem function should have to take into account the probability of arrival. The latter is defined as the probability that a propagule of a particular species will arrive at a particular community. Arrival probability depends on the dispersal ability and the number of propagules of a species, the distance a species needs to travel, and the permeability of the matrix landscape. Current databases, in particular those in northwestern and central Europe now enable robust estimation of arrival probability in plant communities. We suggest a general hypothesis claiming that dispersal limitation according to arrival probability will have ecosystem‐level effects different from those arising due to random arrival. This hypothesis may be rendered more region‐, landscape‐ or ecosystem‐specific by estimating arrival probabilities for different background conditions.     

Long‐term consistency in spatial patterns of primate seed dispersal

Seed dispersal is a key ecological process in tropical forests, with effects on various levels ranging from plant reproductive success to the carbon storage potential of tropical rainforests. On a local and landscape scale, spatial patterns of seed dispersal create the template for the recruitment process and thus influence the population dynamics of plant species. The strength of this influence will depend on the long‐term consistency of spatial patterns of seed dispersal. We examined the long‐term consistency of spatial patterns of seed dispersal with spatially explicit data on seed dispersal by two neotropical primate species, Leontocebus nigrifrons and Saguinus mystax (Callitrichidae), collected during four independent studies between 1994 and 2013. Using distributions of dispersal probability over distances independent of plant species, cumulative dispersal distances, and kernel density estimates, we show that spatial patterns of seed dispersal are highly consistent over time. For a specific plant species, the legume Parkia panurensis, the convergence of cumulative distributions at a distance of 300 m, and the high probability of dispersal within 100 m from source trees coincide with the dimension of the spatial–genetic structure on the embryo/juvenile (300 m) and adult stage (100 m), respectively, of this plant species. Our results are the first demonstration of long‐term consistency of spatial patterns of seed dispersal created by tropical frugivores. Such consistency may translate into idiosyncratic patterns of regeneration.     

Bird‐mediated seed dispersal: reduced digestive efficiency in active birds modulates the dispersal capacity of plant seeds

Plant populations in fragmented ecosystems rely largely on internal dispersal by animals. To unravel the mechanisms underlying this mode of dispersal, an increasing number of experimental feeding studies is carried out. However, while physical activity is known to affect vertebrate digestive processes, almost all current knowledge on mechanisms of internal seed dispersal has been obtained from experiments with resting animals. We investigated how physical activity of the mallard Anas platyrhynchos, probably the quantitatively most important biotic dispersal agent in aquatic habitats in the entire Northern Hemisphere, affects gut passage survival and retention time of ingested plant seeds. We fed seeds of nine common wetland plants to mallards trained to subsequently swim for six hours in a flume tank at different swimming speeds (activity levels). We compared gut passage survival and retention times of seeds against a control treatment with mallards resting in a conventional dry cage. Intact gut passage of seeds increased significantly with mallard activity (up to 80% in the fastest swimming treatment compared to the control), identifying reduced digestive efficiency due to increased metabolic rates as a mechanism enhancing the dispersal potential of ingested seeds. Gut passage speed was modestly accelerated (13% on average) by increased mallard activity, an effect partly obscured by the interaction between seed retention time and probability of digestion. Gut passage acceleration will be more pronounced in digestion‐resilient seed species, thereby modulating their dispersal distances. Our findings imply that seed dispersal potential by mallards calculated from previous experiments with resting birds is highly underestimated, while dispersal distances may be overestimated for some plant species. Similar effects of physical activity on digestive efficiency of mammals suggests that endozoochorous dispersal of plant seeds by vertebrates is more effective and plays a quantitatively more important ecological role in both terrestrial and aquatic ecosystems than previously thought.     

A distance–performance trade‐off in the phenotypic basis of dispersal

Across taxa, individuals vary in how far they disperse, with most individuals staying close to their origin and fewer dispersing long distances. Costs associated with dispersal (e.g., energy, risk) are widely believed to trade off with benefits (e.g., reduced competition, increased reproductive success) to influence dispersal propensity. However, this framework has not been applied to understand variation in dispersal distance, which is instead generally attributed to extrinsic environmental factors. We alternatively hypothesized that variation in dispersal distances results from trade‐offs associated with other aspects of locomotor performance. We tested this hypothesis in the stream salamander Gyrinophilus porphyriticus and found that salamanders that dispersed farther in the field had longer forelimbs but swam at slower velocities under experimental conditions. The reduced swimming performance of long‐distance dispersers likely results from drag imposed by longer forelimbs. Longer forelimbs may facilitate moving longer distances, but the proximate costs associated with reduced swimming performance may help to explain the rarity of long‐distance dispersal. The historical focus on environmental drivers of dispersal distances misses the importance of individual traits and associated trade‐offs among traits affecting locomotion.     

Modelling the effect of size on the aerial dispersal of microorganisms

Aim We investigate the long‐standing question of whether the small size of microbes allows most microbial species to colonize all suitable sites around the globe or whether their ranges are limited by opportunities for dispersal. In this study we use a modelling approach to investigate the effect of size on the probability of between‐continent dispersal using virtual microorganisms in a global model of the Earth’s atmosphere. Location Global. Methods We use a computer model of global atmospheric circulation to investigate the effect of microbe size (effective diameters of 9, 20, 40 and 60 μm) on the probability of aerial dispersal. Results We found that for smaller microbes, once airborne, dispersal is remarkably successful over a 1‐year period. The most striking results are the extensive within‐hemisphere distribution of virtual microbes of 9 and 20 μm diameter and the lack of dispersal between the Northern and Southern Hemispheres during the year‐long time‐scale of our simulations. Main conclusions Above a diameter of 20 μm wind dispersal of virtual microbes between continents becomes increasingly unlikely, and it does not occur at all (within our simulated 1‐year period) for those of 60 μm diameter. Within our simulation, the success of small microbes in long‐distance dispersal is due both to their greater abundance and to their longer time in the atmosphere – once airborne – compared with larger microbes.     

Better nutritional condition changes the distribution of juvenile dispersal distances: an experiment with Spanish imperial eagles

We investigated the distribution of juvenile dispersal distances of a territorial long‐lived species with deferred maturity, the Spanish imperial eagle Aquila adalberti. Here we used a reintroduction program as an experimental approach to test predictions of different hypotheses about the distribution of juvenile dispersal distances: competition and wandering behavior. We determined maximal juvenile dispersal distances of 59 young eagles; 1) 30 wild non‐manipulated individuals, and 2) 29 tranlocated young under an ad libitum feeding program, released with adults breeding in the area. The competitive displacement hypothesis predicts a leptokurtic distribution of distances in wild non‐manipulated young as well as in released young. Under the ‘wandering’ hypothesis, however, a leptokurtic distribution is expected in wild young but a normal distribution would be expected in young released (with adults in the release area), owing to a general improvement in the nutritional status of released young that have been fed ad libitum, as is usual in reintroduction programs. Additionally, a negative relationship between hatching date and dispersal distances is expected in wild young but no relationship in released young under ad libitum feeding. Mean maximum dispersal distances for all the juvenile eagles was 142.8 km. No differences between sexes were found, nor between populations or between wild and reintroduced young. Wild young distances were not normally distributed, being closer to a Poisson distribution. In contrast, released young with adults (under ad libitum feeding) showed a normal distribution. Wild birds showed a significant negative relationship between dispersal distance and hatching date, with young that hatched late in the season dispersing shorter distances. However, released young under ad libitum feeding showed no significant relationship between hatching date and dispersal distance. These results support the ‘wandering’ hypothesis as the main driver of the distribution of dispersal distances.     

Determinants and costs of natal dispersal in a lekking species

Avoidance of competition and inbreeding have been invoked as the major ultimate causes of natal dispersal, but proximate factors such as sex, body condition or birth date can also be important. Natal dispersal is expected to be of particular importance to understanding the ecological and evolutionary implications of dispersal strategies, since 1) numerous evidences suggest that individual differences in dispersal strategies are expressed early in life (i.e. at the onset of dispersal movement), 2) ultimate and proximate factors are more likely to act during this stage and 3) this stage is associated with the highest mortality rates in most vertebrates. We analysed the natal dispersal (hereafter, dispersal) behaviour in 100 marked individuals of a lekking species, the North African houbara bustards Chlamydotis undulata undulata, during four years. We investigated the effects of proximate factors on dispersal pattern and distance, as well as the mortality cost associated with movement using multievent models, allowing uncertainty in sex assignment and mixture of live recaptures and dead recoveries. Overall, males exhibited longer dispersal distances than females, contrary to the common pattern in birds. Moreover, males in poorer body condition moved further than those in better condition, whereas distance was independent of body condition in females. Finally, survival rates during dispersal were lower for females than for males and were negatively correlated with the distances covered with a similar distance‐survival slope in the two sexes. Collectively, our results suggest that 1) there is substantial dispersal cost in both sexes, 2) dispersal is strongly male‐biased, 3) this bias is unlikely to be explained by differential movement costs of each sex, and 4) dispersal differences found across different categories of individuals are in broad agreement with both the inbreeding avoidance and intraspecific competition mechanisms for dispersal.     

Impact of the spatial uncertainty of seed dispersal on tree colonization dynamics in a temperate forest

An aggregated distribution of dispersed seeds may influence the colonization process in tree communities via inflated spatial uncertainty. To evaluate this possibility, we studied 10 tree species in a temperate forest: one primarily barochorous, six anemochorous and two endozoochorous species. A statistical model was developed by combining an empirical seed dispersal kernel with a gamma distribution of seedfall density, with parameters that vary with distance. In the probability density, the fitted models showed that seeds of Fagaceae (primarily barochorous) and Betulaceae (anemochorous) were disseminated locally (i.e. within 60 m of a mother tree), whereas seeds of Acer (anemochorous) and endozoochorous species were transported farther. Greater fecundity compensated for the lower probability of seed dispersal over long distances for some species. Spatial uncertainty in seedfall density was much greater within 60 m of a mother tree than farther away, irrespective of dispersal mode, suggesting that seed dispersal is particularly aggregated in the vicinity of mother trees. Simulation results suggested that such seed dispersal patterns could lead to sites in the vicinity of a tree being occupied by other species that disperse seeds from far away. We speculate that this process could promote coexistence by making the colonization rates of the species more similar on average and equalizing species fitness in this temperate forest community.     

Evolution of condition-dependent dispersal under kin competition

Dispersers often differ in body condition from non-dispersers. The social dominance hypothesis explains dispersal of weak individuals, but it is not yet well understood why strong individuals, which could easily retain their natal site, are sometimes exposed to risky dispersal. Based on the model for dispersal under kin competition by Hamilton and May, we construct a model where dispersal propensity depends on body condition. We consider an annual species that inhabits a patchy environment with varying patch qualities. Offspring body condition corresponds to the quality of the natal patch and competitive ability increases with body condition. Our main general result balances the fitness benefit from not dispersing and retaining the natal patch and the benefit from dispersing and establishing somewhere else. We present four different examples for competition, which all hint that dispersal of strong individuals may be a common outcome under the assumptions of the present model. In three of the examples, the evolutionarily stable dispersal probability is an increasing function of body condition. However, we found an example where, counterintuitively, the evolutionarily stable dispersal probability is a non-monotone function of body condition such that both very weak and very strong individuals disperse with high probability but individuals of intermediate body condition do not disperse at all.     

Variability within families and the evolution of body-condition-dependent dispersal

In a population where body condition varies between and within families, we investigate the evolution of dispersal as a function of body condition ('strength', e.g. body size). Strong individuals are better competitors in a weighted lottery. If body condition does not influence survival during dispersal, then there is no unique evolutionarily stable strategy. Instead, there are infinitely many dispersal strategies that all lead to the same non-dispersing weight in a patch. These strategies are all selectively neutral but determine wildly different relationships between body condition and disposal probability. This may explain why there is no consistent pattern between body condition and dispersal found in empirical studies. If body condition influences survival during dispersal, then neutrality is removed and individuals with higher survival probability disperse. Dispersal may be the competitively weaker individuals if smaller body size helps to avoid dispersal risks.     

Probability of successful larval dispersal declines fivefold over 1 km in a coral reef fish

A central question of marine ecology is, how far do larvae disperse? Coupled biophysical models predict that the probability of successful dispersal declines as a function of distance between populations. Estimates of genetic isolation-by-distance and self-recruitment provide indirect support for this prediction. Here, we conduct the first direct test of this prediction, using data from the well-studied system of clown anemonefish (Amphiprion percula) at Kimbe Island, in Papua New Guinea. Amphiprion percula live in small breeding groups that inhabit sea anemones. These groups can be thought of as populations within a metapopulation. We use the x- and y-coordinates of each anemone to determine the expected distribution of dispersal distances (the distribution of distances between each and every population in the metapopulation). We use parentage analyses to trace recruits back to parents and determine the observed distribution of dispersal distances. Then, we employ a logistic model to (i) compare the observed and expected dispersal distance distributions and (ii) determine the relationship between the probability of successful dispersal and the distance between populations. The observed and expected dispersal distance distributions are significantly different (p < 0.0001). Remarkably, the probability of successful dispersal between populations decreases fivefold over 1 km. This study provides a framework for quantitative investigations of larval dispersal that can be applied to other species. Further, the approach facilitates testing biological and physical hypotheses for the factors influencing larval dispersal in unison, which will advance our understanding of marine population connectivity.     

Evolution of stepping-stone dispersal rates

We present a general model of the evolution of dispersal in a population with any distribution of dispersal distance. We use this model to analyse evolutionarily stable (ES) dispersal rates for the classical island model of dispersal and for three different stepping-stone models. Using general techniques to compute relatedness coefficients in the different dispersal models which we consider, we find that the distribution of dispersal distance may affect the ES dispersal rate when the cost of dispersal is low. In this case the ES dispersal rate increases with the number of demes that can be reached by one dispersal event. However, for increasing cost the ES dispersal rate converges to a value independent of the distribution of dispersal distance. These results are in contrast to previous analyses of similar models. The effects of the size (number of demes) and shape (ratio between the width and the length) of the population on the evolution of dispersal are also studied. We find that larger and more elongated populations lead generally to higher ES dispersal rates. However, both of these effects can only be observed for extreme parameter values (i.e. for very small and very elongated populations). The direct fitness method and the analytical techniques used here to compute relatedness coefficients provide an efficient way to analyse ES strategies in subdivided populations.     

Mutation surfing and the evolution of dispersal during range expansions

A growing body of empirical evidence demonstrates that at an expanding front, there can be strong selection for greater dispersal propensity, whereas recent theory indicates that mutations occurring towards the front of a spatially expanding population can sometimes ‘surf’ to high frequency and spatial extent. Here, we consider the potential interplay between these two processes: what role may mutation surfing play in determining the course of dispersal evolution and how might dispersal evolution itself influence mutation surfing? Using an individual‐based coupled‐map lattice model, we first run simulations to determine the fate of dispersal mutants that occur at an expanding front. Our results highlight that mutants that have a slightly higher dispersal propensity than the wild type always have a higher survival probability than those mutants with a dispersal propensity lower than, or very similar to, the wild type. However, it is not always the case that mutants with very high dispersal propensity have the greatest survival probability. When dispersal mortality is high, mutants of intermediate dispersal survive most often. Interestingly, the rate of dispersal that ultimately evolves at an expanding front is often substantially higher than that which confers a novel mutant with the greatest probability of survival. Second, we run a model in which we allow dispersal to evolve over the course of a range expansion and ask how the fate of a neutral or nonneutral mutant depends upon when and where during the expansion it arises. These simulations highlight that the success of a neutral mutant depends upon the dispersal genotypes that it is associated with. An important consequence of this is that novel mutants that arise at the front of an expansion, and survive, typically end up being associated with more dispersive genotypes than the wild type. These results offer some new insights into causes and the consequences of dispersal evolution during range expansions, and the methodology we have employed can be readily extended to explore the evolutionary dynamics of other life history characteristics.     

Limited dispersal by Nazca boobies Sula granti

We documented natal and breeding dispersal at several spatial scales by Galápagos Nazca boobies Sula granti, a wide‐ranging pelagic seabird. We found exceptionally low degrees of both types of dispersal despite these birds’ vagility. Median natal dispersal distances were 26 m and 105 m for males and females, respectively. Median breeding dispersal distances for both sexes were 0 m. No natal or breeding dispersals occurred from our study site at Punta Cevallos, Isla Española to six other colonies in the Galápagos, but we did document four long‐distance natal dispersals from Punta Cevallos to islands near the South American coast. Recaptures and dead recoveries of ringed birds showed long distance non‐breeding movements to the Central American coast and elsewhere in the eastern Pacific, contrasting with the very limited dispersal to breeding sites.     

Between‐patch natal dispersal declines with increasing natal patch size and distance to other patches in the endangered Southern Dunlin Calidris alpina schinzii

Natal dispersal has profound consequences for populations through the movement of individuals and genes. Habitat fragmentation reduces structural connectivity by decreasing patch size and increasing isolation, but understanding of how this impacts dispersal and the functional connectivity of landscapes is limited because many studies are constrained by the size of the study areas or sample sizes to accurately capture natal dispersal. We quantified natal dispersal probability and natal dispersal distances in a small migratory shorebird, the Southern Dunlin Calidris alpina schinzii, with data from two extensively monitored endangered metapopulations breeding in Sweden and Finland. In both metapopulations philopatry was strong, with individuals returning to or close to their natal patches more often than expected by chance, consistent with the patchy distribution of their breeding habitat. Dispersal probabilities were lower and dispersal distances were shorter in Sweden. These results provide a plausible explanation for the observed inbreeding and population decline of the Swedish population. The differences between Sweden and Finland were explained by patch‐specific differences. Between‐patch dispersal decreased with increasing natal patch size and distance to other patches. Our results suggest that reduced connectivity reduces movements of the philopatric Dunlin, making it vulnerable to the effects of inbreeding. Increasing connectivity between patches should thus be one of the main goals when planning future management. This may be facilitated by creating a network of suitably sized patches (20–100 ha), no more than 20 km apart from each other, from existing active patches that may work as stepping stones for movement, and by increasing nest success and pre‐fledging survival in small patches.     

Breeding dispersal of Eurasian kestrels Falco tinnunculus under temporally fluctuating food abundance

Costs and benefits of dispersal can vary in space and time, depending on environmental factors and individual state. Plastic, condition‐dependent dispersal strategies, in which individuals rely on external cues such as food abundance to adjust their dispersal distances, are therefore expected to evolve in temporally fluctuating environments. We examined factors affecting breeding dispersal distances in Eurasian kestrels Falco tinnunculus subsisting on multi‐annually and cyclically fluctuating voles as their main food. We attempted to avoid traditional bias in dispersal studies by having large study areas and by taking detection probabilities into account. We observed 320 dispersal events of male and 215 events of female kestrels from our study areas in western Finland during 24 yr. After correcting for distance‐specific detection probability, the estimates of mean dispersal distances increased two‐fold being still clearly higher for females than males. Vole abundance in the spring of settlement was more important in determining average dispersal distances than vole abundance in the previous autumn. At the population level (cross‐sectional model), both males and females dispersed longer distances when the spring abundance of their main food (voles) was low compared to when it was abundant, as predicted by the food depletion hypothesis. At the individual level (longitudinal model), only females responded to the food situation by dispersing more when food abundance was low in the spring of settlement. Females also dispersed longer when vole abundance in the previous autumn had been high. Individual males did not respond to vole abundance, which implies that the population level response in males might have been caused by long‐distance dispersers, which breed in the study area only in good vole years. Our results show that the dispersal distances of kestrels at northern latitudes depend both on individual properties (gender, age, and possibly individual tendency to disperse) and environmental conditions (temporal variation in main food abundance).