Plant dispersal, neighbourhood size and isolation by distance

A theoretical relationship between isolation by distance or spatial genetic structure (SGS) and seed and pollen dispersal is tested using extensive spatial-temporal simulations. Although for animals Wright's neighbourhood size N(e) = 4pisigma(2)(t) has been ascertained also, where sigma(2)(t) is the axial variance of distances between parents and offspring, and it was recently confirmed that N(e) = 4pi(sigma(2)(f) + sigma(2)(m))/2 when dispersal of females and males differ, the situation for plants had not been established. This article shows that for a very wide range of conditions, neighbourhood size defined by Crawford's formula N(e) = 4pi(sigma(2)(s) + sigma(2)(p)/2) fully determines SGS, even when dispersal variances of seed (sigma(2)(s)) and pollen sigma(2)(p)) differ strongly. Further, self-fertilization with rate s acts as zero-distance pollen dispersal, and N(e) = 4pi[sigma(2)(s) + sigma(2)(p)(1 - s)/2] fully determines SGS, for most cases where there are both likely parameter values and substantial SGS. Moreover, for most cases, there is a loglinear relationship, I(1) = 0.587 - 0.117 ln(N(e)), between SGS, as measured by I(1), Moran's coefficient for adjacent individuals, and N(e). However, there are several biologically significant exceptions, namely for very low or large N(e), SGS exceeds the loglinear values. There are also important exceptions to Crawford's formula. First, plants with low seed dispersal, high outcross pollen dispersal and high selfing rate show larger SGS than predicted. Second, in plants with very low (near zero) seed dispersal, selfing decreases SGS, opposite expectations. Finally, in some cases seed dispersal is more critical than pollen dispersal, in a manner inconsistent with Crawford's formula.     

Molecular and ecological evidence for small-scale isolation by distance in an endangered damselfly, Coenagrion mercuriale

Coenagrion mercuriale (Charpentier) (Odonata: Zygoptera) is one of Europe's most threatened damselflies and is listed in the European Habitats directive. We combined an intensive mark-release-recapture (MRR) study with a microsatellite-based genetic analysis for C. mercuriale from the Itchen Valley, UK, as part of an effort to understand the dispersal characteristics of this protected species. MRR data indicate that adult damselflies are highly sedentary, with only a low frequency of interpatch movement that is predominantly to neighbouring sites. This restricted dispersal leads to significant genetic differentiation throughout most of the Itchen Valley, except between areas of continuous habitat, and isolation by distance (IBD), even though the core populations are separated by less than 10 km. An urban area separating some sites had a strong effect on the spatial genetic structure. Average pairwise relatedness between individual damselflies is positive at short distances, reflecting fine-scale genetic clustering and IBD both within- and between-habitat patches. Damselflies from a fragmented habitat have higher average kinship than those from a large continuous population, probably because of poorer dispersal and localized breeding in the former. Although indirect estimates of gene flow must be interpreted with caution, it is encouraging that our results indicate that the spatial pattern of genetic variation matches closely with that expected from direct observations of movement. These data are further discussed with respect to possible barriers to dispersal within the study site and the ecology and conservation of C. mercuriale. To our knowledge, this is the first report of fine-scale genetic structuring in any zygopteran species.     

Pervasive selection or is it…? why are FST outliers sometimes so frequent?

It is now common for population geneticists to estimate F_ST for a large number of loci across the genome, before testing for selected loci as being outliers to the F_ST distribution. One surprising result of such F_ST scans is the often high proportion (>1% and sometimes >10%) of outliers detected, and this is often interpreted as evidence for pervasive local adaptation. In this issue of Molecular Ecolog, Fourcade et al. ( 2013 ) observe that a particularly high rate of F_ST outliers has often been found in river organisms, such as fishes or damselflies, despite there being no obvious reason why selection should affect a larger proportion of the genomes of these organisms. Using computer simulations, Fourcade et al. ( 2013 ) show that the strong correlation in co‐ancestry produced in long one‐dimensional landscapes (such as rivers, valleys, peninsulas, oceanic ridges or coastlines) greatly increases the neutral variance in F_ST, especially when the landscape is further reticulated into fractal networks. As a consequence, outlier tests have a high rate of false positives, unless this correlation can be taken into account. Fourcade et al.'s study highlights an extreme case of the general problem, first noticed by Robertson ( 1975a , b ) and Nei & Maruyama ( 1975 ), that correlated co‐ancestry inflates the neutral variance in F_ST when compared to its expectation under an island model of population structure. Similar warnings about the validity of outlier tests have appeared regularly since then but have not been widely cited in the recent genomics literature. We further emphasize that F_ST outliers can arise in many different ways and that outlier tests are not designed for situations where the genetic architecture of local adaptation involves many loci.     

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.     

Habitat connectivity is determined by the scale of habitat loss and dispersal strategy

Understanding factors that ameliorate the impact of habitat loss is a major focus of conservation research. One key factor influencing species persistence and evolution is the ability to disperse across increasingly patchy landscapes. Here we ask whether interpatch distance (a proxy for habitat loss) and dispersal strategy can interact to form thresholds where connectivity breaks down. We assayed dispersal across a range of interpatch distances in fruit flies carrying allelic variants of a gene known to underlie differences in dispersal strategy. Dispersal‐limited flies experienced a distinct negative threshold in connectivity at greater interpatch distances, and this was not observed in more dispersive flies. Consequently, this differential response of dispersal‐limited and more dispersive flies to decreasing connectivity suggests that habitat loss could have important implications on the evolution and maintenance of genetic variation underlying dispersal strategy.     

Does size matter for dispersal distance?

Aim The aim of this study is to answer the questions: (1) do small organisms disperse farther than large, or vice versa; and (2) does the observed pattern differ for passive and active dispersers? These questions are central to several themes in biogeography (including microbial biogeography), macroecology, metacommunity ecology and conservation biology. Location The meta‐analysis was conducted using published data collected worldwide. Methods We collected and analysed 795 data values in the peer‐reviewed literature for direct observations of both maximal dispersal distance and mass of the dispersing organisms (e.g. seeds, not trees). Analysed taxa ranged in size from bacteria to whales. We applied macroecology analyses based on null models (using Monte Carlo randomizations) to test patterns relative to specific hypotheses. Results Collected dispersal distance and mass data spanned 9 and 21 orders of magnitude, respectively. Active dispersers dispersed significantly farther (P < 0.001) and were significantly greater in mass (P < 0.001) than passive dispersers. Overall, size matters: larger active dispersers attained greater maximum observed dispersal distances than smaller active dispersers. In contrast, passive‐disperser distances were random with respect to propagule mass, but not uniformly random, in part due to sparse data available for tiny propagules. Conclusions Size is important to maximal dispersal distance for active dispersers, but not for passive dispersers. Claims that microbes disperse widely cannot be tested by current data based on direct observations of dispersal: indirect approaches will need to be applied. Distance–mass relationships should contribute to a resolution of neutral and niche‐based metacommunity theories by helping scale expectations for dispersal limitation. Also, distance–mass relationships should inform analyses of latitudinal species richness and conservation biology topics such as fragmentation, umbrella species and taxonomic homogenization.     

Effects of dynamic landscape elements on fish dispersal: the example of creek chub (Semotilus atromaculatus)

Barriers along a watercourse and interconnections between drainage systems are dynamic landscape elements that are expected to play major roles in the dispersal and genetic structure of fish species. The objective of this study was to assess the role of these elements using creek chub ( Semotilus atromaculatus ) in the Mastigouche Wildlife Reserve (Québec, Canada) as model. Numerous impassable waterfalls and interconnections among drainage systems were inferred with geographic information systems and confirmed de visu . The analysis of 32 populations using seven nuclear microsatellites revealed the presence of three genetically distinct groups. Some groups were found upstream of impassable barriers and in adjacent portions of distinct drainage systems. Admixture among groups was also detected in some populations. Constraining phylogenetic procedures as well as Mantel correlation tests confirmed that the genetic structure is more likely to result from interconnections between the drainage systems than from the permanent network. This study indicates that landscape elements such as interconnections are of major importance for circumventing impassable barriers and colonizing lakes that are otherwise inaccessible. Such an approach could be relevant for determining the origins of fish species (i.e. native vs. introduced) in the context of conservation.     

Using relatedness networks to infer contemporary dispersal: Application to the endangered mammal Galemys pyrenaicus

Information about the degree of contemporary dispersal is important when trying to understand how populations interchange individuals and identify the specific barriers that prevent these movements. In the case of endangered species, this can represent crucial information when designing appropriate conservation strategies. Here we analyse relatedness between individuals from different localities and use these data to infer whether dispersal occurred in recent generations. We applied this approach to the Pyrenean desman (Galemys pyrenaicus), a semiaquatic and endangered species endemic to the Iberian Peninsula. We studied this species in four primary rivers in the Iberian Range, where two ancient mitochondrial lineages are separated by a strict contact zone, suggesting the existence of complex dispersal patterns. Using next‐generation sequencing, we obtained 912 SNPs from each specimen and estimated relatedness values between them. While relatedness networks were dense within each river, we found surprisingly few relationships between individuals from different rivers despite their close proximity in some cases, indicating much lower dispersal between rivers compared to dispersal within a single river. In agreement with this result, the degree of inbreeding was exceedingly high in most individuals. These data show that relatedness information can be crucial to understand the contemporary dispersal patterns and conservation status of specific populations of endangered species.     

Current approaches using genetic distances produce poor estimates of landscape resistance to interindividual dispersal

Landscape resistance reflects how difficult it is for genes to move across an area with particular attributes (e.g. land cover, slope). An increasingly popular approach to estimate resistance uses Mantel and partial Mantel tests or causal modelling to relate observed genetic distances to effective distances under alternative sets of resistance parameters. Relatively few alternative sets of resistance parameters are tested, leading to relatively poor coverage of the parameter space. Although this approach does not explicitly model key stochastic processes of gene flow, including mating, dispersal, drift and inheritance, bias and precision of the resulting resistance parameters have not been assessed. We formally describe the most commonly used model as a set of equations and provide a formal approach for estimating resistance parameters. Our optimization finds the maximum Mantel r when an optimum exists and identifies the same resistance values as current approaches when the alternatives evaluated are near the optimum. Unfortunately, even where an optimum existed, estimates from the most commonly used model were imprecise and were typically much smaller than the simulated true resistance to dispersal. Causal modelling using Mantel significance tests also typically failed to support the true resistance to dispersal values. For a large range of scenarios, current approaches using a simple correlational model between genetic and effective distances do not yield accurate estimates of resistance to dispersal. We suggest that analysts consider the processes important to gene flow for their study species, model those processes explicitly and evaluate the quality of estimates resulting from their model.     

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.     

Seed dispersal distance classes and dispersal modes for the European flora

Motivation

Although dispersal ability is one of the key features determining the spatial dynamics of plant populations and the structure of plant communities, it is also one of the traits for which we still lack data for most species. We compiled a comprehensive dataset of seed dispersal distance classes and predominant dispersal modes for most European vascular plants. Our seed dispersal dataset can be used in functional biogeography, dynamic vegetation modelling and ecological studies at local to continental scales.

Main Types of Variables Contained

Species were classified into seven ordered classes with similar dispersal distances estimated based on the predominant dispersal mode, the morphology of dispersal units (diaspores or propagules), life form, plant height, seed mass, habitat and known dispersal by humans. We evaluated our results by comparing them with dispersal distances calculated using the ‘dispeRsal’ function in R.

Spatial Location

Europe.

Time Period

Present.

Major Taxa and Level of Measurement

The seed dispersal dataset contains information on dispersal distance classes and the predominant dispersal mode for 10,327 most frequent and locally dominant European vascular plant species.

Software Format

Data are available in .csv format.     

Spatial graphs highlight how multi-generational dispersal shapes landscape genetic patterns

Current approaches that compare spatial genetic structure of a given species and the dispersal of its mobile phase can detect a mismatch between both patterns mainly due to processes acting at different temporal scales. Genetic structure result from gene flow and other evolutionary and demographic processes over many generations, while dispersal predicted from the mobile phase often represents solely one generation on a single time-step. In this study, we present a spatial graph approach to landscape genetics that extends connectivity networks with a stepping-stone model to represent dispersal between suitable habitat patches over multiple generations. We illustrate the approach with the case of the striped red mullet Mullus surmuletus in the Mediterranean Sea. The genetic connectivity of M. surmuletus was not correlate with the estimated dispersal probability over one generation, but with the stepping-stone estimate of larval dispersal, revealing the temporal scale of connectivity across the Mediterranean Sea. Our results highlight the importance of considering multiple generations and different time scales when relating demographic and genetic connectivity. The spatial graph of genetic distances further untangles intra-population genetic structure revealing the Siculo-Tunisian Strait as an important corridor rather than a barrier for gene flow between the Western- and Eastern Mediterranean basins, and identifying Mediterranean islands as important stepping-stones for gene flow between continental populations. Our approach can be easily extended to other systems and environments.     

Unique evolutionary trajectories in repeated adaptation to hydrogen sulphide‐toxic habitats of a neotropical fish (Poecilia mexicana)

Replicated ecological gradients are prime systems to study processes of molecular evolution underlying ecological divergence. Here, we investigated the repeated adaptation of the neotropical fish Poecilia mexicana to habitats containing toxic hydrogen sulphide (H₂S) and compared two population pairs of sulphide‐adapted and ancestral fish by sequencing population pools of >200 individuals (Pool‐Seq). We inferred the evolutionary processes shaping divergence and tested the hypothesis of increase of parallelism from SNPs to molecular pathways. Coalescence analyses showed that the divergence occurred in the face of substantial bidirectional gene flow. Population divergence involved many short, widely dispersed regions across the genome. Analyses of allele frequency spectra suggest that differentiation at most loci was driven by divergent selection, followed by a selection‐mediated reduction of gene flow. Reconstructing allelic state changes suggested that selection acted mainly upon de novo mutations in the sulphide‐adapted populations. Using a corrected Jaccard index to quantify parallel evolution, we found a negligible proportion of statistically significant parallel evolution of J_corr = 0.0032 at the level of SNPs, divergent genome regions (J_corr = 0.0061) and genes therein (J_corr = 0.0091). At the level of metabolic pathways, the overlap was J_corr = 0.2545, indicating increasing parallelism with increasing level of biological integration. The majority of pathways contained positively selected genes in both sulphide populations. Hence, adaptation to sulphidic habitats necessitated adjustments throughout the genome. The largely unique evolutionary trajectories may be explained by a high proportion of de novo mutations driving the divergence. Our findings favour Gould's view that evolution is often the unrepeatable result of stochastic events with highly contingent effects.     

Population structure and dispersal patterns in Scottish Golden Eagles Aquila chrysaetos revealed by molecular genetic analysis of territorial birds

Conservation management of species distributed across fragmented habitats requires consideration of population genetic structure and relative levels of genetic diversity throughout the relevant geographical range. The Golden Eagle Aquila chrysaetos is monitored within Scotland to ensure its survival in the face of land‐use pressure, persecution and future climate change. In this study we constructed DNA profiles for 271 individual birds using a collection of over 1600 moulted feathers collected from 148 territories, representing 34% of known Scottish territories in the largest population genetic study of Golden Eagles undertaken to date. The results, based on data from 10 nuclear microsatellite loci, revealed previously unreported genetic structure between the islands of the Outer Hebrides and the rest of Scotland (F_ST = 0.03), together with evidence of reduced genetic diversity in the Outer Hebridean population compared with mainland Scotland. Analysis of gene flow supports a hypothesis of limited, predominantly male‐mediated, dispersal from the Outer Hebrides to mainland Scotland. The persistence of this pattern is discussed with respect to variation in population density and persecution pressure across Scotland. A finding of non‐random mating within the Outer Hebrides is interpreted as evidence of natal philopatry that was revealed by more intensive sampling in these islands, and is likely to be accentuated by the apparent degree of isolation of the islands from the rest of Scotland.     

Genetic assignment of recruits reveals short‐ and long‐distance larval dispersal in Pocillopora damicornis on the Great Barrier Reef

Understanding connectivity of coral populations among and within reefs over ecologically significant timescales is essential for developing evidence‐based management strategies, including the design of marineprotected areas. Here, we present the first assessment of contemporary connectivity among populations of two Molecular Operational Taxonomic Units (MOTUs) of the brooding coral Pocillopora damicornis. We used individual‐based genetic assignment methods to identify the proportions of philopatric and migrant larval recruits, settling over 12 months at sites around Lizard Island (northern Great Barrier Reef [GBR]) and over 24 months at sites around the Palms Islands (central GBR). Overall, we found spatially and temporally variable rates of self‐recruitment and dispersal, demonstrating the importance of variation in local physical characteristics in driving dispersal processes. Recruitment patterns and inferred dispersal distances differed between the two P. damicornis MOTUs, with type α recruits exhibiting predominantly philopatric recruitment, while the majority of type β recruits were either migrants from identified putative source populations or assumed migrants based on genetic exclusion from all known populations. While P. damicornis invests much energy into brooding clonal larvae, we found that only 15% and 7% of type α and type β recruits, respectively, were clones of sampled adult colonies or other recruits, challenging the hypothesis that reproduction is predominantly asexual in this species on the GBR. We explain high rates of self‐recruitment and low rates of clonality in these MOTUs by suggesting that locally retained larvae originate predominantly from spawned gametes, while brooded larvae are mainly vagabonds.