Determining parentage and relatedness from genetic markers sheds light on patterns of marine larval dispersal

Population connectivity, the extent to which geographically separated subpopulations exchange individuals and are demographically linked, is important to the scientific management of marine living resources. In theory, the design of a marine protected area, for example, depends on an explicit understanding of how dispersal of planktonic larvae affects metapopulation structure and dynamics ( Botsford et al. 2001 ). In practice, for most marine metazoans with planktonic larvae, the mean and variance of the distances that larvae disperse are unobservable quantities, owing to the small sizes of larvae and the very large volumes through which they are distributed. Simulation of dispersal kernels with models that incorporate oceanography and limited aspects of larval biology and behaviour, coupled with field studies of larval distribution, abundance, and settlement, have provided the best available approaches to date for understanding connectivity of marine populations ( Cowen et al. 2006 ). On the other hand, marine population connectivity has often been judged by spatial variation in the frequencies of alleles and genotypes, although the inherent limitations of this indirect approach to measuring larval dispersal have often been overlooked ( Hedgecock et al. 2007 ). More recently, researchers have turned to genetic methods and highly polymorphic markers that can provide direct evidence of population connectivity in the form of parentage or relatedness of recruits (e.g. Jones et al. 2005 ). In this issue, Christie et al. (2010) provide a particularly elegant example, in which both indirect and novel direct genetic methods are used to determine the major ecological processes shaping dispersal patterns of larval bicolour damselfish Stegastes partitus, a common and widespread reef fish species in the Caribbean Basin ( Fig. 1 ).

Figure 1 Open in figure viewer PowerPoint The bicolour damselfish Stegastes partitus shows substantial self‐recruitment of juveniles to their natal coral reef habitat. Below, a male guarding an artificial nest made from PVC pipe; differential reproductive success of parents or differential survival of egg clutches or the larvae that hatch from them may account for signals of sweepstakes reproductive success in this species (photo credits: top, Bill Harward; bottom, Darren Johnson).     

DNA fingerprinting validates seed dispersal curves from observational studies in the neotropical legume parkia

Background

Determining the distances over which seeds are dispersed is a crucial component for examining spatial patterns of seed dispersal and their consequences for plant reproductive success and population structure. However, following the fate of individual seeds after removal from the source tree till deposition at a distant place is generally extremely difficult. Here we provide a comparison of observationally and genetically determined seed dispersal distances and dispersal curves in a Neotropical animal-plant system.

Methodology/Principal Findings

In a field study on the dispersal of seeds of three Parkia (Fabaceae) species by two Neotropical primate species, Saguinus fuscicollis and Saguinus mystax, in Peruvian Amazonia, we observationally determined dispersal distances. These dispersal distances were then validated through DNA fingerprinting, by matching DNA from the maternally derived seed coat to DNA from potential source trees. We found that dispersal distances are strongly right-skewed, and that distributions obtained through observational and genetic methods and fitted distributions do not differ significantly from each other.

Conclusions/Significance

Our study showed that seed dispersal distances can be reliably estimated through observational methods when a strict criterion for inclusion of seeds is observed. Furthermore, dispersal distances produced by the two primate species indicated that these primates fulfil one of the criteria for efficient seed dispersers. Finally, our study demonstrated that DNA extraction methods so far employed for temperate plant species can be successfully used for hard-seeded tropical plants.     

Biological and environmental effects on fine-scale seed dispersal of an invasive tree in a secondary subtropical forest

Dispersal abilities of invading species emerge from the interaction between the species and some features of the target community. Ligustrum lucidum is a tree species invading different ecosystems. Major spatial patterns of Ligustrum invasions and their ecological consequences have been analyzed, but no study addressed the dispersal process at a fine scale, assessing the effects of different biological and environmental factors. Ligustrum lucidum is an ornithochoric species. The structure of the environment determines bird movements and thus affects seed dispersal. We used inverse modeling to analyze bird-mediated dispersal of L. lucidum seeds in a secondary Yungas forest and surrounding crop-fields. We assessed the effects of egestion mode (regurgitation and defecation) and tree density (as an environment character) on seed dispersal. Seed dispersal presented different spatial patterns depending on the egestion mode. Tree density was positively associated with the number of regurgitated dispersed seeds and negatively associated with the number of defecated dispersed seeds. In both cases, dispersal distance increased in open areas, but absence of perches inhibited seed arrival. Thus, spread of L. lucidum is facilitated in open areas with some trees; inside the native forest, short distance dispersal facilitates the gradual invasion by this exotic species. Our results suggest that processes like crop abandonment and forest succession, which are active in subtropical montane systems, may facilitate L. lucidum invasion. Our seed dispersal models should be combined with actual distribution maps of L. lucidum to identify areas vulnerable to new invasions.     

Local population genetic structure of the montane caddisfly Drusus discolor is driven by overland dispersal and spatial scaling

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The evolution of dispersal

A non-local model for dispersal with continuous time and space is carefully justified and discussed. The necessary mathematical background is developed and we point out some interesting and challenging problems. While the basic model is not new, a spread parameter (effectively the width of the dispersal kernel) has been introduced along with a conventional rate paramter, and we compare their competitive advantages and disadvantages in a spatially heterogeneous environment. We show that, as in the case of reaction-diffusion models, for fixed spread slower rates of diffusion are always optimal. However, fixing the dispersal rate and varying the spread while assuming a constant cost of dispersal leads to more complicated results. For example, in a fairly general setting given two phenotypes with different, but small spread, the smaller spread is selected while in the case of large spread the larger spread is selected. S. Martinez was partially supported by Fondecyt 1020126 and Fondecyt Lineas Complementarias 8000010. K. Mischaikow was supported in part by NSF Grant DMS 0107396. Key words or phases:Non-local dispersal – Integral kernel – Evolution of dispersal     

Pollen dispersal and gene flow within and into a population of the alpine monocarpic plant Campanula thyrsoides

Background and Aims

Gene flow by seed and pollen largely shapes the genetic structure within and among plant populations. Seed dispersal is often strongly spatially restricted, making gene flow primarily dependent on pollen dispersal within and into populations. To understand distance-dependent pollination success, pollen dispersal and gene flow were studied within and into a population of the alpine monocarpic perennial Campanula thyrsoides.

Methods

A paternity analysis was performed on sampled seed families using microsatellites, genotyping 22 flowering adults and 331 germinated offspring to estimate gene flow, and pollen analogues were used to estimate pollen dispersal. The focal population was situated among 23 genetically differentiated populations on a subalpine mountain plateau (<10 km²) in central Switzerland.

Key Results

Paternity analysis assigned 110 offspring (33·2 %) to a specific pollen donor (i.e. ‘father’) in the focal population. Mean pollination distance was 17·4 m for these offspring, and the pollen dispersal curve based on positive LOD scores of all 331 offspring was strongly decreasing with distance. The paternal contribution from 20–35 offspring (6·0–10·5 %) originated outside the population, probably from nearby populations on the plateau. Multiple potential fathers were assigned to each of 186 offspring (56·2 %). The pollination distance to ‘mother’ plants was negatively affected by the mothers'' degree of spatial isolation in the population. Variability in male mating success was not related to the degree of isolation of father plants.

Conclusions

Pollen dispersal patterns within the C. thyrsoides population are affected by spatial positioning of flowering individuals and pollen dispersal may therefore contribute to the course of evolution of populations of this species. Pollen dispersal into the population was high but apparently not strong enough to prevent the previously described substantial among-population differentiation on the plateau, which may be due to the monocarpic perenniality of this species.     

Evaluating hypotheses about dispersal in a vulnerable butterfly

Sound management of species requires reliable estimates of dispersal. Indeed, dispersal of individuals among local populations is a key factor in the biology and persistence of local populations and metapopulations. Here, the small-scale dispersal pattern of a vulnerable species, the endemic Sardinian chalk hill blue butterfly, was studied by applying capture–recapture multistate models and a model selection based on AIC values. Model parameters were survival, capture and movement probabilities. The model selection showed that (a) survival probability of individuals varied between sexes, (b) capture probability varied between sexes and among patches, and (c) movement probability varied with direction. The probability of movement among adjacent local populations was generally low and ranged from 0.009 to 0.212. Movement probabilities were subsequently modeled using data on interpatch distance and donor patch population size or area. The ultrastructural biology-based models turned out to be the most appropriate models for inference, showing that dispersal decreases with increasing interpatch distance and increasing donor patch population size or area, and suggesting that butterfly dispersal is affected by patch geometry and the presence of conspecifics. The application of multistate models, the model selection approach, and ultrastructural modeling allowed testing the validity of some general hypotheses related to dispersal in metapopulations and helped elucidate the butterfly small-scale dispersal pattern.     

A potential role for overland dispersal in shaping aquatic invertebrate communities in arid regions

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Evolution of dispersal distance

The problem of how often to disperse in a randomly fluctuating environment has long been investigated, primarily using patch models with uniform dispersal. Here, we consider the problem of choice of seed size for plants in a stable environment when there is a trade off between survivability and dispersal range. Ezoe (J Theor Biol 190:287–293, 1998) and Levin and Muller-Landau (Evol Ecol Res 2:409–435, 2000) approached this problem using models that were essentially deterministic, and used calculus to find optimal dispersal parameters. Here we follow Hiebeler (Theor Pop Biol 66:205–218, 2004) and use a stochastic spatial model to study the competition of different dispersal strategies. Most work on such systems is done by simulation or nonrigorous methods such as pair approximation. Here, we use machinery developed by Cox et al. (Voter model perturbations and reaction diffusion equations 2011) to rigorously and explicitly compute evolutionarily stable strategies.     

Endozoochory by beetles: a novel seed dispersal mechanism

Background and Aims

Due in part to biophysical sized-related constraints, insects unlike vertebrates are seldom expected to act as primary seed dispersers via ingestion of fruits and seeds (endozoochory). The Mediterranean parasitic plant Cytinus hypocistis, however, possesses some characteristics that may facilitate endozoochory by beetles. By combining a long-term field study with experimental manipulation, we tested whether C. hypocistis seeds are endozoochorously dispersed by beetles.

Methods

Field studies were carried out over 4 years on six populations in southern Spain. We recorded the rate of natural fruit consumption by beetles, the extent of beetle movement, beetle behaviour and the relative importance of C. hypocistis fruits in beetle diet.

Key Results

The tenebrionid beetle Pimelia costata was an important disperser of C. hypocistis seeds, consuming up to 17·5 % of fruits per population. Forty-six per cent of beetles captured in the field consumed C. hypocistis fruits, with up to 31 seeds found in individual beetle frass. An assessment of seeds following passage through the gut of beetles indicated that seeds remained intact and viable and that the proportion of viable seeds from beetle frass was not significantly different from that of seeds collected directly from fruits.

Conclusions

A novel plant–animal interaction is revealed; endozoochory by beetles may facilitate the dispersal of viable seeds after passage through the gut away from the parent plant to potentially favourable underground sites offering a high probability of germination and establishment success. Such an ecological role has until now been attributed only to vertebrates. Future studies should consider more widely the putative role of fruit and seed ingestion by invertebrates as a dispersal mechanism, particularly for those plant species that possess small seeds.     

Joint evolution of sex ratio and dispersal: conditions for higher dispersal rates from good habitats

We analyze models of evolution of sex ratio conditional on habitat quality and with sex specific dispersal. Previous analysis concluded that the main constraint on sex ratio is habitat choice and leads to overproduction of the most dispersing sex in low quality habitat. Here, we analyze three models with finite local populations and show that constraints on sex ratio can balance constraints on habitat choice. In the first model, dispersal rates are fixed. In the second, sex specific dispersal can evolve independently of the habitat quality. These models suggests that sex ratio evolution can lead to higher global dispersal rates (mean of male and female dispersal rates) from high quality habitats. In the last model dispersal evolves conditionally with both sex and habitat. Our models suggests that conditions for overproduction of the most dispersing sex in high quality habitat are frequent. The predictions of the models with evolving dispersal contrast with patterns generally described in nature. We discuss possible reasons of this difference.     

Metacommunity organisation,spatial extent and dispersal in aquatic systems: patterns,processes and prospects

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Temporal and nonlinear dispersal patterns of <Emphasis Type="Italic">Ludwigia hexapetala</Emphasis> in a regulated river

Rivers are vulnerable to biological invasion due to hydrologic connectivity, which facilitates post-entry movement of aquatic plant propagules by water currents. Ecological and watershed factors may influence spatial and temporal dispersal patterns. Field-based data on dispersal could improve risk assessment models and management responses. Ludwigia hexapetala, an invasive emergent macrophyte, provides a case study for understanding dispersal patterns throughout a watershed. The species spreads via hydrochory and is increasingly imposing detrimental ecological and economic impacts within watersheds of the United States and Europe. We investigated morphology of shoot fragments and their dispersal in the Russian River watershed of California, capturing shoot fragments of L. hexapetala during repeated summer surveys at five locations in the river and quantifying their morphological traits that predict establishment success. Highly variable capture counts suggest the importance of pulse disturbance events in local dispersal of L. hexapetala. Unexpectedly, dispersing propagule pressure was nonlinear, with more shoot fragments captured in the middle rather than lower river. Captured fragments in the middle river were twice the length of fragments captured in the lower river and bore 83% more stem nodes, characteristics associated with greater establishment success. Our results support development of spatially targeted management, outreach, and prevention efforts that could lead to decreased propagule pressure in the watershed.     

Female breeding dispersal in wolverines,a solitary carnivore with high territorial fidelity

Individuals’ fidelity to an area provides insight into the stability of the spatial and temporal organisation of animals. Territorial fidelity is often influenced by reproductive success, age, the dispersion and predictability of resources, and intraspecific competition. We examined between-year territorial fidelity in wolverines (Gulo gulo), using location data from 47 individuals collected during 1993–2013 in northern Sweden, to assess the stability of the spatial organisation of this solitary carnivore. For females, we also determined residency status from 1 year to the next. The study population is characterized by a stable distribution of resident individuals, with both males and females showing higher fidelity at the total territory level compared to more intensively used core areas. In 86% of the yearly residency status estimates (n?=?122), the female remained stationary. In the remaining 14% of the cases, females either vacated their territory (8% of residency statuses), or expanded into a neighbouring territory (6% of residency statuses). We documented six cases of breeding dispersal, representing one of the few known cases of breeding dispersal in long-lived large mammals. We suggest that this high territorial fidelity is enabled by wolverines’ caching and scavenging behaviours, which buffer the unpredictable and large spatiotemporal variation in resource abundance in this low-productivity area. Breeding dispersal may occur due to competition for high-quality territories in this saturated population, where females are forced to abandon their territory by competitors or bequeath territories to offspring. This study further highlights the complexity of the social and spatial dynamics for solitary carnivores.     

Seed dispersal distances by ant partners reflect preferential recruitment patterns in two ant-dispersed sedges

An important feature of seed dispersal mutualism is the differentiation of dispersal-related seed traits (dispersal syndrome), which potentially contribute to partitioning of both seed dispersers and regeneration sites among sympatric plants. Yet, the selective factors underlying the diversity in dispersal syndromes are largely unknown. The differential requirements for seed dispersal distances are often proposed as a main factor in plant adaptations to disperser animals. Focusing on two sympatric ant-dispersed sedges Carex lanceolata and Carex tristachya (Cyperaceae), we tested the association of the adaptation to different dispersers with requirements for seed dispersal distances. We found that C. lanceolata was more frequently dispersed by the large ant Formica japonica (which had relatively long dispersal distances compared with other smaller ants) than by C. tristachya, and this was caused by the higher seed attractiveness of C. lanceolata to F. japonica. Pot experiments manipulating adult-to-seedling distances showed that isolation from conspecific adults only benefited C. lanceolata seedlings, and C. tristachya seedlings were not affected. These results support the importance of differential requirements for seed dispersal distances as a factor underlying the diversity in dispersal syndromes among animal-dispersed plants.     

Long-distance dispersal of tree seeds by wind

Some mechanisms that promote long-distance dispersal of tree seeds by wind are explored. Winged seeds must be lifted above the canopy by updrafts to have a chance of further dispersal in high velocity horizontal winds aloft or in landscape-scale convection cells. Shear-induced turbulent eddies of a scale up to one-third of canopy height provide a lifting mechanism. Preliminary data suggest that all seeds of a given species may be viable candidates for uplift and long-distance dispersal, despite the evidence that slow-falling seeds are dispersed farther under any given wind conditions. Turbulence is argued more often and more extensively to advance long-distance dispersal than to retard it. Seeds may take advantage of Bernoulli sailing to move with faster than average winds. Elasticity of branches and trees may play a role in regulating the release of seeds into unusually favorable winds. Dispersal is at least biphasic, and the study of long-distance dispersal calls for mixed models and mixed methods of gathering data.     

First evidence of epizoochorous seed dispersal by golden snub-nosed monkeys (<Emphasis Type="Italic">Rhinopithecus roxellana</Emphasis>) in temperate forest

Although many primates are identified as effective endozoochorous seed dispersers in forest ecosystems, epizoochorous seed dispersal by primates has generally been overlooked. In this study, we report epizoochorous seed dispersal in a group of free-ranging golden snub-nosed monkeys (Rhinopithecus roxellana) residing in the temperate forests of central China by identifying seeds carried by 12 well-habituated individuals. The results showed a total of 1920 seeds (five families, seven genera) belonging to eight plant species attached to the monkeys’ fur; the three most abundant species were Geum aleppicum (54% of the total), Torilis japonica (17%), and Agrimonia pilosa (14%). The majority of seeds (95.3%) that attached to the monkeys’ fur had special morphologies such as hairs, hooks, or awns. We also found that the quantity of seeds attached to the fur was not significantly different by age-sex class, even though adult males have very long fur. Our study provides the first empirical evidence of epizoochorous seed dispersal by primates and suggests the role of primates in seed dispersal may be greater than previously assumed.     

Role of male dispersal in the evolution of female altruistic behavior in viscous populations

A computer simulation was conducted to examine the effect of differential dispersal of sexes on the evolution of altruism in viscous populations. First, a basic model, which was regarded as a purely viscous population model, was constructed. The model was assumed to be the same as the simulation model of Wilson etal. (1992), except that it assumed sexual reproduction and that only females show altruistic behavior toward females. For the basic model, altruism could not evolve when b/Nc, where b is the benefit of the altruism to the recipient, c is the cost to the altruist, and N is the number of interacting neighbors. The male dispersal model I assumed that females disperse to nine neighboring sites including the natal site, but males disperse to eight sites farther than females do. For this model, altruistic alleles could evolve when b/N was equal to c or b/N was slightly smaller than c only when the male dispersal distance was slightly larger than those of females. The male dispersal model II assumed that the male dispersal distance follows a normal probability distribution. The Vole model was based on actual data of the gray-sided vole, Clethironomys rufocanus bedfordiae, whose frequency distribution of dispersal distance was similar to a normal distribution. For these models, altruism could evolve under the condition that b/N was slightly smaller than c when the dispersal distances of males were larger than those of females. The results indicate that the differential dispersal of sexes, in which females are philopatric and males disperse farther than females, can somewhat increase the probability of spreading altruistic alleles in viscous populations.     

Analysis of disruptive selection in subdivided populations

Background

Analytical methods have been proposed to determine whether there are evolutionarily stable strategies (ESS) for a trait of ecological significance, or whether there is disruptive selection in a population approaching a candidate ESS. These criteria do not take into account all consequences of small patch size in populations with limited dispersal.

Results

We derive local stability conditions which account for the consequences of small and constant patch size. All results are derived from considering R_m, the overall production of successful emigrants from a patch initially colonized by a single mutant immigrant. Further, the results are interpreted in term of concepts of inclusive fitness theory. The condition for convergence to an evolutionarily stable strategy is proportional to some previous expressions for inclusive fitness. The condition for evolutionary stability stricto sensu takes into account effects of selection on relatedness, which cannot be neglected. It is function of the relatedness between pairs of genes in a neutral model and also of a three-genes relationship. Based on these results, I analyze basic models of dispersal and of competition for resources. In the latter scenario there are cases of global instability despite local stability. The results are developed for haploid island models with constant patch size, but the techniques demonstrated here would apply to more general scenarios with an island mode of dispersal.

Conclusions

The results allow to identity and to analyze the relative importance of the different selective pressures involved. They bridge the gap between the modelling frameworks that have led to the R_m concept and to inclusive fitness.

     

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

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