The importance of long-distance dispersal in biodiversity conservation

Dispersal is universally considered important for biodiversity conservation. However, the significance of long‐ as opposed to short‐distance dispersal is insufficiently recognized in the conservation context. Long‐distance dispersal (LDD) events, although typically rare, are crucial to population spread and to maintenance of genetic connectivity. The main threats to global biodiversity involve excessive LDD of elements alien to ecosystems and insufficient dispersal of native species, for example, because of habitat fragmentation. In this paper, we attempt to bridge the gap in the treatment of LDD by reviewing the conservation issues for which LDD is most important. We then demonstrate how taking LDD into consideration can improve conservation management decisions.     

Long distance dispersal and the fate of a gene from the colonization front

There is an increasing recognition that long distance dispersal (LDD) plays a key role in establishing spatial genetic structure during colonization. Recent works, focused on short distance dispersal, demonstrated that a neutral mutation arising at the colonization front can either ‘surf’ with the wave front and reach high frequencies or stay near its place of origin at low frequencies. Here, we examine how LDD, and more generally the shape of the dispersal kernel, modifies this phenomenon and how the width of the colonization corridor affects the fate of the mutation. We demonstrate that when LDD events are more frequent, the ‘surfing phenomenon’ is less frequent, probably because any alleles can get far ahead from the colonization front and preclude the invasion by others alleles, thus leading to an attenuation of the diversity loss. We also demonstrate that the width of the colonization corridor influences the fate of the mutation, wide spaces decreasing the probability of invasion. Overall, the genetic structure of diversity resulted not only from LDD but also particularly from the shape of the dispersal kernel.     

Deriving dispersal distances from genetic data.

Dispersal is one of the most important factors determining the genetic structure of a population, but good data on dispersal distances are rare because it is difficult to observe a large sample of dispersal events. However, genetic data contain unbiased information about the average dispersal distances in species with a strong sex bias in their dispersal rates. By plotting the genetic similarity between members of the philopatric sex against some measure of the distance between them, the resulting regression line can be used for estimating how far dispersing individuals of the opposite sex have moved before settling. Dispersers showing low genetic similarity to members of the opposite sex will on average have originated from further away. Applying this method to a microsatellite dataset from lions (Panthera leo) shows that their average dispersal distance is 1.3 home ranges with a 95% confidence interval of 0.4-3.0 home ranges. These results are consistent with direct observations of dispersal from our study population and others. In this case, direct observations of dispersal distance were not detectably biased by a failure to detect long-range dispersal, which is thought to be a common problem in the estimation of dispersal distance.     

Contrasting effects of long distance seed dispersal on genetic diversity during range expansion

Currently many attempts are made to reconstruct the colonization history of plant species after the last ice age. A surprising finding is that during the colonization phase genetic diversity did not decrease as much as expected. In this paper we examine whether long distance seed dispersal events could play a role in the unexpected maintenance of genetic diversity during range expansion. This study is based on simulations carried out with a maternally inherited haploid locus using a cellular automaton. The simulations reveal a close relationship between the frequency of long distance seed dispersal events and the amount of genetic diversity preserved during colonization. In particular, when the colonized region is narrow, a complete loss of genetic diversity results from the occurrence of very rare long distance dispersal (LDD) events. We call this phenomenon the 'embolism effect'. However, slightly higher rates of LDD events reverse this effect, up to the point that diversity is better preserved than in a pure diffusion model. This phenomenon is linked to the reorganization of the genetic structure during colonization and is called the 'reshuffling effect'.     

Testing Darwin's transoceanic dispersal hypothesis for the inland nettle family (Urticaceae)

Dispersal is a fundamental ecological process, yet demonstrating the occurrence and importance of long‐distance dispersal (LDD) remains difficult, having rarely been examined for widespread, non‐coastal plants. To address this issue, we integrated phylogenetic, molecular dating, biogeographical, ecological, seed biology and oceanographic data for the inland Urticaceae. We found that Urticaceae originated in Eurasia c. 69 Ma, followed by ≥ 92 LDD events between landmasses. Under experimental conditions, seeds of many Urticaceae floated for > 220 days, and remained viable after 10 months in seawater, long enough for most detected LDD events, according to oceanographic current modelling. Ecological traits analyses indicated that preferences for disturbed habitats might facilitate LDD. Nearly half of all LDD events involved dioecious taxa, so population establishment in dioecious Urticaceae requires multiple seeds, or occasional selfing. Our work shows that seawater LDD played an important role in shaping the geographical distributions of Urticaceae, providing empirical evidence for Darwin's transoceanic dispersal hypothesis.     

Range expansion and retraction along a moving contact zone has no effect on the genetic diversity of two passerine birds

Disentangling the factors shaping species distributions remains a central goal in biogeography, ecology and evolutionary biology. The extrinsic pressures that may facilitate range shifts, such as climatic factors or biotic interactions are well known. However, in contrast, the possible intrinsic factors are manifold and hard to generalize across taxa. Recently, several theoretical studies have investigated the consequences of moving range borders on genetic diversity. However, empirical studies that support or refute these theoretical predictions are scarce. Moving contact zones between parapatric sister species are suitable models to test these hypotheses. Changes in genetic diversity can be tested simultaneously along the expanding and receding edges of two species of the contact zone while accounting for intra‐specific effects (e.g. introgression). The two Old World warblers Hippolais polyglotta and H. icterina form a narrow moving contact zone, where interspecific interactions are suspected to be the main factor shaping this zone. We investigated the population genetic structure of both species along a transect ranging from the core range of the expanding H. polyglotta across the contact zone and far into the range of the receding H. icterina. The theoretical predictions of changes in genetic diversity at the range edges were tested. No gradual change in genetic diversity was detected for both the expanding and the receding range margin. Furthermore, no genetic structure was found in either species supporting the hypothesis that long distance dispersal (LDD) occurs frequently due to the high mobility of these long‐distance migrants. The results suggest that when dispersal propensity is high and accompanied by frequent LDD events, then neither an enrichment nor a depletion of alleles along moving range edges would be detected. This these species as the probability to retain genetic diversity during exogenous induced range shifts is high in such mobile species.     

Worldwide long‐distance dispersal favored by epizoochorous traits in the biogeographic history of Omphalodeae (Boraginaceae)

Biogeographic dispersal is supported by numerous phylogenetic results. In particular, transoceanic dispersal, rather than vicariance, is suggested for some plant lineages despite current long distances between America and Europe. However, few studies on the biogeographic history of plants have also studied the role of diaspore syndromes in long‐distance dispersal (LDD). Species of the tribe Omphalodeae (Boraginaceae) offer a suitable study system because the species have a wide variety of diaspore traits related to LDD and different lineages conform to patched worldwide distributions on three distant continents (Europe, America and New Zealand). Our aim is to reconstruct the biogeographical history of the Omphalodeae and to investigate the role of diaspore traits favoring LDD and current geographic distributions. To this end, a time‐calibrated phylogeny with 29 of 32 species described for Omphalodeae was reconstructed using biogeographical analyses (BioGeoBEARS, Lagrange) and models (DEC and DIVA) under different scenarios of land connectivity. Character‐state reconstruction (SIMMAP) and diversification rate estimations of the main lineages were also performed. The main result is that epizoochorous traits have been the ancestral state of LDD syndromes in most clades. An early diversification age of the tribe is inferred in the Western Mediterranean during late Oligocene. Colonization of the New World by Omphalodeae, followed by fast lineage differentiation, took place sometime in the Oligocene‐Miocene boundary, as already inferred for other angiosperm genera. In contrast, colonization of remote islands (New Zealand, Juan Fernández) occurred considerably later in the Miocene‐Pliocene boundary.     

Importance of functional traits and regional species pool in predicting long-distance dispersal in savanna ecosystems

Long-distance dispersal (LDD) of plants is difficult to measure but disproportionately important for various ecological and evolutionary processes. Dispersal of seeds of gallery-forest trees in savanna provides an opportunity for the study of colonisation processes and species coexistence driven by LDD. Investigations were carried out on 91 isolated trees along four gallery forests sampled in the Biosphere Reserve of Pendjari, Benin. The abundance of adult trees within nearest gallery forest was combined with functional traits (species maximum height, seed weight, morphological adaptation for dispersal by wind, water, birds and mammals) to explain the floristic composition of forest seedlings and saplings under isolated trees and in savanna. Stepwise negative binomial regression was used to identify the most significant variables explaining abundance of seedlings and saplings beneath isolated trees and in savanna and then derive colonisation from seedlings and persistence from saplings. The maximum height of species and seed weight explained the highest proportion of variance in species colonisation. Morphological dispersal syndromes by wind and birds had poor explanatory importance. Species rare in gallery forest had higher potential to colonise new environments through LDD whilst abundant species had higher persistence abilities. Contrary to the predictions of the seedling-size effect, small-seeded species dominated the sapling stage. The findings revealed the strong dependence of LDD and subsequent colonisation and persistence processes on species traits specialised for a variety of dispersal vectors. They also suggest that LDD towards isolated trees established far away from gallery forest can be difficult.     

Using stable isotopes to trace long-distance dispersal in birds and other taxa

The study of long‐distance dispersal (LDD) in animals may be advanced by recent applications of stable isotope analyses designed to track migratory organisms and to link populations throughout their annual cycle. This approach depends on there being enough isotopic difference in tissues among potential source populations such that individuals can be unequivocally assigned to their source. The isotopic mapping of such populations will be feasible only for species occurring in relatively few disjunct populations. However, the identification of isotopic outliers within known populations will be an extremely useful first step in the forensic application of stable isotopes to identify dispersal in general, and LDD in particular. The use of deuterium isotope analysis (δD) of tissues that can be assigned to its source (e.g. feather moult or its hair growth location) has provided a recent breakthrough in our ability to associate individuals with geographical origins at continental scales. The combination of this stable isotope with others and the ultimate combination of a variety of techniques, including the measurement of trace elements and molecular genetics markers, will undoubtedly improve resolution. The isotopic cataloguing of known history (i.e. philopatric) individuals within populations will be an important step in applying isotope techniques to evaluating LDD in any species. For aquatic insects, the isotopic marking of large numbers of individuals is possible through isotopic enrichment of local food webs using labelled compounds.     

Going against the flow: a case for upstream dispersal and detection of uncommon dispersal events

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A first step towards inferring levels of long-distance dispersal during past expansions

Improving the realism of spatially explicit demographic models is important for better inferring the history of past populations and for understanding the genetic bases of adaptation and speciation. One particular type of demographic event to take into account is long-distance dispersal (LDD). The goals of this study are to explore the impact of various levels of LDD on genetic diversity and to show to what extent LDD levels can be correctly inferred from multilocus data sets using an approximate Bayesian computation approach. We therefore incorporated LDD into a 2D stepping stone forward simulation framework coupled to a coalescent backward simulation step to generate genetic diversity at 100 microsatellite markers under various demographic conditions relevant to recent human evolution. Our results confirm that LDD considerably increases genetic diversity within demes and decreases levels of diversity between demes. By controlling the spatial occurrence of LDD, it appears that LDD events occurring during a phase of range expansion into new territories are more important in maintaining genetic diversity than those occurring in the wake of the expansion or when colonization is over. We also show that it is possible to infer whether LDD has occurred during a range expansion, but our results suggest that one can only approximately estimate the extent of LDD based on genetic summary statistics.     

Long-distance dispersal research: building a network of yellow brick roads

This special issue of Diversity and Distributions presents six papers that contribute to the assembly of a general research agenda for studying long‐distance dispersal (LDD) across a variety of taxonomic groups (e.g. birds, fish, aquatic invertebrates and plants), ecosystems (e.g. terrestrial and marine ecosystems, wetlands and grasslands) and thematic fields (e.g. biological transport, marine biology, biogeochemistry and biodiversity conservation). This editorial emphasizes the need to develop a network integrating different research approaches (‘yellow brick roads’) to address the great challenge (‘finding the end of the rainbow’) of quantifying, understanding and predicting LDD and its implications. I review the key avenues for future research suggested in the special issue contributions, and stress the critical importance of properly considering the spatial and temporal scales relevant to the process and system of interests. I propose combining absolute and proportional definitions of LDD as a default practice in any investigation of LDD processes. When LDD is defined primarily by an absolute critical distance that characterizes key feature(s) of the system of interest, a quantitative assessment of the proportion of dispersal events expected to move beyond this critical threshold distance should also be provided. When LDD is defined primarily by a certain small fraction of dispersal events that travel longer than all others, an estimate of the absolute distance associated with this high percentile at the tail of the dispersal curve should also be added.     

Working at the interface of phylogenetics and population genetics: a biogeographical analysis of Triaenops spp. (Chiroptera: Hipposideridae)

New applications of genetic data to questions of historical biogeography have revolutionized our understanding of how organisms have come to occupy their present distributions. Phylogenetic methods in combination with divergence time estimation can reveal biogeographical centres of origin, differentiate between hypotheses of vicariance and dispersal, and reveal the directionality of dispersal events. Despite their power, however, phylogenetic methods can sometimes yield patterns that are compatible with multiple, equally well-supported biogeographical hypotheses. In such cases, additional approaches must be integrated to differentiate among conflicting dispersal hypotheses. Here, we use a synthetic approach that draws upon the analytical strengths of coalescent and population genetic methods to augment phylogenetic analyses in order to assess the biogeographical history of Madagascar's Triaenops bats (Chiroptera: Hipposideridae). Phylogenetic analyses of mitochondrial DNA sequence data for Malagasy and east African Triaenops reveal a pattern that equally supports two competing hypotheses. While the phylogeny cannot determine whether Africa or Madagascar was the centre of origin for the species investigated, it serves as the essential backbone for the application of coalescent and population genetic methods. From the application of these methods, we conclude that a hypothesis of two independent but unidirectional dispersal events from Africa to Madagascar is best supported by the data.     

Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds

Although Darwin pioneered the study of long‐distance dispersal (LDD) of aquatic invertebrates via waterbirds, it remains in its infancy as a modern discipline. A handful of recent studies have quantified internal or external transport in the field, confirming that a variety of long‐distance migrants carry invertebrates both internally and externally. These studies show that variation in the morphology of vectors influences the frequency and size of propagules transported, and suggest that more invertebrate groups disperse via birds than was previously thought. Dispersal limitation has mainly been investigated for zooplankton in small experimental systems from which waterbirds were effectively excluded, and the extent of such limitation for invertebrate populations in wetlands interconnected by waterbird movements remains unclear. We expect that the spatial and temporal scales at which dispersal limitation constrains geographical ranges, species richness and genetic structure of invertebrates depends partly on the density of migratory birds using the area. Birds may have a major role in the expansion of exotic species. We propose several avenues for future research. There is a particular need for more quantitative studies of LDD by birds that will enable modellers to assess its role in maintaining invertebrate biodiversity among increasingly fragmented wetlands and in the face of climate change, as well as in the spread of invasive species.     

Genetic discontinuities and disequilibria in recently established populations of the plant pathogenic fungus Mycosphaerella fijiensis

Dispersal processes of fungal plant pathogens can be inferred from analysis of spatial genetic structures resulting from recent range expansion. The relative importance of long‐distance dispersal (LDD) events vs. gradual dispersal in shaping population structures depends on the geographical scale considered. The fungus Mycosphaerella fijiensis, pathogenic on banana, is an example of a recent worldwide epidemic. Founder effects in this species were detected at both global and continental scale, suggesting stochastic spread of the disease through LDD events. In this study, we analysed the structure of M. fijiensis populations in two recently (∼1979–1980) colonized areas in Costa Rica and Cameroon. Isolates collected in 10–15 sites distributed along a ∼250‐ to 300‐ km‐long transect in each country were analysed using 19 microsatellite markers. We detected low‐to‐moderate genetic differentiation among populations in both countries and isolation by distance in Cameroon. Combined with historical data, these observations suggest continuous range expansion at the scale of banana‐production area through gradual dispersal of spores. However, both countries displayed specific additional signatures of colonization: a sharp discontinuity in gene frequencies was observed along the Cameroon transect, while the Costa Rican populations seemed not yet to have reached genetic equilibrium. These differences in the genetic characteristics of M. fijiensis populations in two recently colonized areas are discussed in the light of historical data on disease spread and ecological data on landscape features.     

Migratory strategies of waterbirds shape the continental‐scale dispersal of aquatic organisms

Long distance dispersal (LDD) of propagules is an important determinant of population dynamics, community structuring and biodiversity distribution at landscape, and sometimes continental, scale. Although migratory animals are potential LDD vectors, migratory movement data have never been integrated in estimates of propagule dispersal distances and LDD probability. Here we integrated migratory movement data of two waterbird species (mallard and teal) over two continents (Europe and North America) and gut retention time of different propagules to build a simple mechanistic model of passive dispersal of aquatic plants and zooplankton. Distance and frequency of migratory movements differed both between waterbird species and continents, which in turn resulted in changes in the shapes of propagule dispersal curves. Dispersal distances and the frequency of LDD events (generated by migratory movements) were mainly determined by the disperser species and, to a lesser extent, by the continent. The gut retention time of propagules also exerted a significant effect, which was mediated by the propagule characteristics (e.g. seeds were dispersed farther than Artemia cysts). All estimated dispersal curves were skewed towards local‐scale dispersal and, although dispersal distances were lower than previous estimates based only on the vector flight speed, had fat tails produced by LDD events that ranged from 230 to 1209 km. Our results suggest that propagule dispersal curves are determined by the migratory strategy of the disperser species, the region (or flyway) through which the disperser population moves, and the propagule characteristics. Waterbirds in particular may frequently link wetlands separated by hundreds of kilometres, contributing to the maintenance of biodiversity and, given the large geographic scale of the dispersal events, to the readjustment of species distributions in the face of climate change.     

Building genetic networks using relatedness information: a novel approach for the estimation of dispersal and characterization of group structure in social animals

Natal dispersal is an important life history trait driving variation in individual fitness, and therefore, a proper understanding of the factors underlying dispersal behaviour is critical to many fields including population dynamics, behavioural ecology and conservation biology. However, individual dispersal patterns remain difficult to quantify despite many years of research using direct and indirect methods. Here, we quantify dispersal in a single intensively studied population of the cooperatively breeding chestnut-crowned babbler (Pomatostomus ruficeps) using genetic networks created from the combination of pairwise relatedness data and social networking methods and compare this to dispersal estimates from re-sighting data. This novel approach not only identifies movements between social groups within our study sites but also provides an estimation of immigration rates of individuals originating outside the study site. Both genetic and re-sighting data indicated that dispersal was strongly female biased, but the magnitude of dispersal estimates was much greater using genetic data. This suggests that many previous studies relying on mark-recapture data may have significantly underestimated dispersal. An analysis of spatial genetic structure within the sampled population also supports the idea that females are more dispersive, with females having no structure beyond the bounds of their own social group, while male genetic structure expands for 750 m from their social group. Although the genetic network approach we have used is an excellent tool for visualizing the social and genetic microstructure of social animals and identifying dispersers, our results also indicate the importance of applying them in parallel with behavioural and life history data.     

Mechanisms of long-distance seed dispersal

Growing recognition of the importance of long-distance dispersal (LDD) of plant seeds for various ecological and evolutionary processes has led to an upsurge of research into the mechanisms underlying LDD. We summarize these findings by formulating six generalizations stating that LDD is generally more common in open terrestrial landscapes, and is typically driven by large and migratory animals, extreme meteorological phenomena, ocean currents and human transportation, each transporting a variety of seed morphologies. LDD is often associated with unusual behavior of the standard vector inferred from plant dispersal morphology, or mediated by nonstandard vectors. To advance our understanding of LDD, we advocate a vector-based research approach that identifies the significant LDD vectors and quantifies how environmental conditions modify their actions.     

The population genetic structure of clonal organisms generated by exponentially bounded and fat-tailed dispersal

Long-distance dispersal (LDD) plays an important role in many population processes like colonization, range expansion, and epidemics. LDD of small particles like fungal spores is often a result of turbulent wind dispersal and is best described by functions with power-law behavior in the tails ("fat tailed"). The influence of fat-tailed LDD on population genetic structure is reported in this article. In computer simulations, the population structure generated by power-law dispersal with exponents in the range of -2 to -1, in distinct contrast to that generated by exponential dispersal, has a fractal structure. As the power-law exponent becomes smaller, the distribution of individual genotypes becomes more self-similar at different scales. Common statistics like GST are not well suited to summarizing differences between the population genetic structures. Instead, fractal and self-similarity statistics demonstrated differences in structure arising from fat-tailed and exponential dispersal. When dispersal is fat tailed, a log-log plot of the Simpson index against distance between subpopulations has an approximately constant gradient over a large range of spatial scales. The fractal dimension D2 is linearly inversely related to the power-law exponent, with a slope of approximately -2. In a large simulation arena, fat-tailed LDD allows colonization of the entire space by all genotypes whereas exponentially bounded dispersal eventually confines all descendants of a single clonal lineage to a relatively small area.     

Intercontinental long‐distance seed dispersal across the Mediterranean Basin explains population genetic structure of a bird‐dispersed shrub

Long‐distance dispersal (LDD) is a pivotal process for plants determining their range of distribution and promoting gene flow among distant populations. Most fleshy‐fruited species rely on frugivorous vertebrates to disperse their seeds across the landscape. While LDD events are difficult to record, a few ecological studies have shown that birds move a sizeable number of ingested seeds across geographic barriers, such as sea straits. The foraging movements of migrant frugivores across distant populations, including those separated by geographic barriers, creates a constant flow of propagules that in turn shapes the spatial distributions of the genetic variation in populations. Here, we have analysed the genetic diversity and structure of 74 populations of Pistacia lentiscus, a fleshy‐fruited shrub widely distributed in the Mediterranean Basin, to elucidate whether the Mediterranean Sea acts as a geographic barrier or alternatively whether migratory frugivorous birds promote gene flow among populations located on both sides of the sea. Our results show reduced genetic distances among populations, including intercontinental populations, and they show a significant genetic structure across an eastern‐western axis. These findings are consistent with known bird migratory routes that connect the European and African continents following a north‐southwards direction during the fruiting season of many fleshy‐fruited plants. Further, approximate Bayesian analysis failed to explain the observed patterns as a result of historical population migrations at the end of Last Glacial Maximum. Therefore, anthropic and/or climatic changes that would disrupt the migratory routes of frugivorous birds might have genetic consequences for the plant species they feed upon.